Abstract
The aim of this study was to adapt and evaluate laser Doppler perfusion monitoring (LDPM) together with custom-designed brain probes and software for continuous recording of cerebral microcirculation in patients undergoing neurosurgery. The LDPM system was used to record perfusion and backscattered light (TLI). These parameters were displayed together with the extracted heart rate (HR), pulsatility index (PI) and signal trends from adjustable time intervals. Technical evaluation was done on skin during thermal provocation. Clinical measurements were performed on ten patients undergoing brain tumour surgery. Data from 76 tissue sites were captured with a length varying between 10 s to 15 min. Statistical comparisons were done using Mann–Whitney tests. Grey and tumour tissue could be separated from white matter using the TLI signal (p < 0.05). The perfusion was significantly higher in grey and tumour tissue compared to white matter (p < 0.005). LDPM was successfully used as an intraoperative tool for monitoring local blood flow and additional parameters linked to cerebral microcirculation (perfusion, TLI, HR and PI) during tumour resection. The systems stability opens up for studies in the postoperative care of patients with, for example, traumatic brain injury or subarachnoid haemorrhage.
Similar content being viewed by others
References
Arshi B, Mack WJ, Emanuel B (2013) Invasive and noninvasive multimodal bedside monitoring in subarachnoid hemorrhage: a review of techniques and available data. Neurol Res Int 2013:987934. doi:10.1155/2013/987934
Barazangi N, Hemphill JC 3rd (2008) Advanced cerebral monitoring in neurocritical care. Neurol India 56(4):405–414
Barone DG, Czosnyka M (2014) Brain monitoring: Do we need a hole? An update on invasive and noninvasive brain monitoring modalities. Sci World J 2014:795762. doi:10.1155/2014/795762
Bellner J, Romner B, Reinstrup P, Kristiansson KA, Ryding E, Brandt L (2004) Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP). Surgical neurology 62(1):45–51. doi:10.1016/j.surneu.2003.12.007 (discussion 51)
Czosnyka M, Pickard JD (2004) Monitoring and interpretation of intracranial pressure. J Neurol Neurosurg Psychiatry 75(6):813–821
Dias C, Maia I, Cerejo A, Varsos G, Smielewski P, Paiva JA, Czosnyka M (2013) Pressures, flow, and brain oxygenation during plateau waves of intracranial pressure. Neurocrit Care. doi:10.1007/s12028-013-9918-y
Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, Tolias C, Oliveira-Ferreira AI, Fabricius M, Hartings JA, Vajkoczy P, Lauritzen M, Dirnagl U, Bohner G, Strong AJ (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132(Pt 7):1866–1881. doi:10.1093/brain/awp102
Ellika SK, Jain R, Patel SC, Scarpace L, Schultz LR, Rock JP, Mikkelsen T (2007) Role of perfusion CT in glioma grading and comparison with conventional MR imaging features. AJNR Am J Neuroradiol 28(10):1981–1987. doi:10.3174/ajnr.A0688
Giller CA, Liu HL, Gurnani P, Victor S, Yasdani U, German DC (2003) Validation of a near-infrared probe for detection of thin intracranial white matter structures. J Neurosurg 98:1299–1306
Gosling RG, King DH (1974) Arterial assessment by Doppler-shift ultrasound. Proc R Soc Med 67(6 Pt 1):447–449
Haberl RL, Villringer A, Dirnagl U (1993) Applicability of laser-Doppler flowmetry for cerebral blood flow monitoring in neurological intensive care. Acta Neurochir Suppl 59:64–68
Haj-Hosseini N, Richter J, Andersson-Engels S, Wårdell K (2010) Optical touch pointer for fluorescence guided glioblastoma resection using 5-aminolevulinic acid. Lasers Surg Med 42(1):9–14
Hillman EM (2007) Optical brain imaging in vivo: techniques and applications from animal to man. J Biomed Opt 12(5):051402
Hillman J, Sturnegk P, Yonas H, Heron J, Sandborg M, Gunnarsson T, Mellergard P (2005) Bedside monitoring of CBF with xenon-CT and a mobile scanner: a novel method in neurointensive care. Br J Neurosurg 19(5):395–401. doi:10.1080/02688690500389898
Jacobs P, Kowatsch R (1993) Sterrad Sterilization System: a new technology for instrument sterilization. Endosc Surg Allied Technol 1(1):57–58
Jakobsson A, Nilsson GE (1993) Prediction of sampling depth and photon pathlength in laser Doppler flowmetry. Med Biol Eng Comput 31(3):301–307
Johansson JD, Blomstedt P, Haj-Hosseini N, Bergenheim AT, Eriksson O, Wårdell K (2009) Combined diffuse light reflectance and electrical impedance measurements as a navigation aid in deep brain surgery. Stereotact Funct Neurosurg 87(2):105–113
Johansson JD, Fredriksson I, Wårdell K, Eriksson O (2009) Simulation of reflected light intensity changes during navigation and radio-frequency lesioning in the brain. J Biomed Opt 14(4):044040
Karlsson MG, Casimir-Ahn H, Lönn U, Wårdell K (2003) Analysis and processing of laser Doppler perfusion monitoring signals recorded from the beating heart. Med Biol Eng Comput 41(3):255–262
Keller E, Froehlich J, Muroi C, Sikorski C, Muser M (2011) Neuromonitoring in intensive care: a new brain tissue probe for combined monitoring of intracranial pressure (ICP) cerebral blood flow (CBF) and oxygenation. Acta Neurochir Suppl 110(Pt 2):217–220. doi:10.1007/978-3-7091-0356-2_39
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109. doi:10.1007/s00401-007-0243-4
Nasrallah I, Dubroff J (2013) An overview of PET neuroimaging. Semin Nucl Med 43(6):449–461. doi:10.1053/j.semnuclmed.2013.06.003
Nilsson GE, Tenland T, Oberg PA (1980) Evaluation of a laser Doppler flowmeter for measurement of tissue blood flow. IEEE Trans Bio-med Eng 27(10):597–604. doi:10.1109/TBME.1980.326582
Nilsson GE, Salerud GE, Strömberg NOT, Wårdell K (2003) Laser Doppler perfusion monitoring and imaging. In: Vo-Dinh T (ed) Biomedical Photonics Handbook, Chap. 15. CRC Press, p 11–24
Parthasarathy AB, Weber EL, Richards LM, Fox DJ, Dunn AK (2010) Laser speckle contrast imaging of cerebral blood flow in humans during neurosurgery: a pilot clinical study. J Biomed Opt 15(6):066030. doi:10.1117/1.3526368
Raabe A, Van De Ville D, Leutenegger M, Szelenyi A, Hattingen E, Gerlach R, Seifert V, Hauger C, Lopez A, Leitgeb R, Unser M, Martin-Williams EJ, Lasser T (2009) Laser Doppler imaging for intraoperative human brain mapping. NeuroImage 44(4):1284–1289. doi:10.1016/j.neuroimage.2008.10.049
Rejmstad P, Akesson G, Hillman J, Wardell K (2012) A laser Doppler system for monitoring of intracerebral microcirculation. In: Conference Proceedings : Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference 2012:1988–1991. doi:10.1109/EMBC.2012.6346346
Richter JC, Haj-Hosseini N, Andersson-Engel S, Wardell K (2011) Fluorescence spectroscopy measurements in ultrasonic navigated resection of malignant brain tumors. Lasers Surg Med 43(1):8–14. doi:10.1002/lsm.21022
Rostami E, Engquist H, Enblad P (2014) Imaging of cerebral blood flow in patients with severe traumatic brain injury in the neurointensive care. Front Neurol 5:114. doi:10.3389/fneur.2014.00114
Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7(5):392–401. doi:10.1016/S1470-2045(06)70665-9
Su XW, Guan Y, Barnes M, Clark JB, Myers JL, Undar A (2011) Improved cerebral oxygen saturation and blood flow pulsatility with pulsatile perfusion during pediatric cardiopulmonary bypass. Pediatr Res 70(2):181–185. doi:10.1038/pr.2011.406
Tarumi T, Ayaz Khan M, Liu J, Tseng BM, Parker R, Riley J, Tinajero C, Zhang R (2014) Cerebral hemodynamics in normal aging: central artery stiffness, wave reflection, and pressure pulsatility. J Cereb Blood Flow Metab. doi:10.1038/jcbfm.2014.44
Wardell K, Jakobsson A, Nilsson GE (1993) Laser Doppler perfusion imaging by dynamic light scattering. IEEE Trans Bio-med Eng 40(4):309–316. doi:10.1109/10.222322
Wårdell K, Braverman IM, Silverman DG, Nilsson GE (1994) Spatial heterogeneity in normal skin perfusion recorded with laser Doppler imaging and flowmetry. Microvasc Res 48(1):26–38
Wårdell K, Blomstedt P, Richter J, Antonsson J, Eriksson O, Zsigmond P, Bergenheim AT, Hariz MI (2007) Intracerebral microvascular measurements during deep brain stimulation implantation using laser Doppler perfusion monitoring. Stereotact Funct Neurosurg 85(6):279–286
Wårdell K, Zsigmond P, Richter J, Hemm S (2013) Relationship between laser Doppler signals and anatomy during deep brain stimulation electrode implantation toward the ventral intermediate nucleus and subthalamic nucleus. Neurosurgery 72(2 Suppl Operative):ons127–ons140. doi:10.1227/NEU.0b013e31827e5821
Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228(2):523–532. doi:10.1148/radiol.2282020409
Winkler MK, Chassidim Y, Lublinsky S, Revankar GS, Major S, Kang EJ, Oliveira-Ferreira AI, Woitzik J, Sandow N, Scheel M, Friedman A, Dreier JP (2012) Impaired neurovascular coupling to ictal epileptic activity and spreading depolarization in a patient with subarachnoid hemorrhage: possible link to blood-brain barrier dysfunction. Epilepsia 53(Suppl 6):22–30. doi:10.1111/j.1528-1167.2012.03699.x
You J, Du C, Volkow ND, Pan Y (2014) Optical coherence Doppler tomography for quantitative cerebral blood flow imaging. Biomed Opt Exp 5(9):3217–3230. doi:10.1364/BOE.5.003217
Zweifel C, Dias C, Smielewski P, Czosnyka M (2014) Continuous time-domain monitoring of cerebral autoregulation in neurocritical care. Med Eng Phys. doi:10.1016/j.medengphy.2014.03.002
Acknowledgments
The authors would like to thank the clinical staff at the Neurosurgical Department of Linköping University Hospital for their help during the surgical measurements. The authors also acknowledge research engineer Mats Andersson and Per Sveider at the Department of Biomedical Engineering for skilful fabrication of the custom optical probes. This study was supported by the Swedish Research Council (Grant No. 6212-010-4216).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rejmstad, P., Åkesson, G., Åneman, O. et al. A laser Doppler system for monitoring cerebral microcirculation: implementation and evaluation during neurosurgery. Med Biol Eng Comput 54, 123–131 (2016). https://doi.org/10.1007/s11517-015-1332-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11517-015-1332-5