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Intraoperative visualization of cerebral oxygenation using hyperspectral image data: a two-dimensional mapping method

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International Journal of Computer Assisted Radiology and Surgery Aims and scope Submit manuscript

Abstract

Purpose

Superficial temporal artery (STA)—middle cerebral artery (MCA) bypass is an important technique for cerebrovascular reconstruction. Intraoperative hemodynamic imaging is needed to perform cerebrovascular reconstruction safely and effectively. Optical intrinsic signal (OIS) imaging is commonly used for assessing cerebral hemodynamics in experimental studies, because it can provide high-resolution mapping images. However, OIS is not used clinically due to algorithm, instrumentation and spectral resolution limitations. We tested the feasibility of a hyperspectral camera (HSC) for assessment of cortical hemodynamics with spectral imaging of the cerebral cortex in rats and in vivo humans.

Methods

A hyperspectral camera (HSC) was tested in a rat model of cerebral ischemia (middle cerebral artery occlusion) and during human revascularization surgery (STA–MCA anastomosis). Changes in cortical oxygen saturation were derived from spectral imaging data (400–800 nm) collected by exposing the cortex to Xenon light. Reflected light was sampled using the HSC. The system was then tested intraoperatively during superficial temporal artery to middle cerebral artery anastomosis procedures. Comparison with single-photon emission computed tomography (SPECT) imaging data was done.

Results

During middle cerebral artery occlusion in rats, the HSC technique showed a significant decrease in cortical oxygen saturation in the ischemic hemisphere. In clinical cases, the cortical oxygen saturation was increased after STA–MCA anastomosis, which agreed with the SPECT imaging data.

Conclusion

Continuous collection of imaging spectroscopic data is feasible and may provide reliable quantification of the hemodynamic responses in the brain. The HSC system may be useful for monitoring intraoperative changes in cortical surface hemodynamics during revascularization procedures in humans.

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References

  1. Mendelowitsch A, Sekhar LN, Clemente R, Shuaib A (1997) EC-IC bypass improves chronic ischemia in a patient with moyamoya disease secondary to sickle cell disease: an in vivo microdialysis study. Neurol Res 19(1):66–70

    PubMed  CAS  Google Scholar 

  2. Ishikawa T, Houkin K, Kamiyama H, Abe H (1997) Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke; J Cereb Circul 28(6):1170–1173

    Article  CAS  Google Scholar 

  3. Rajamani K, Chaturvedi S (2007) Prevention of ischemic stroke: surgery. Curr Drug Targets 8(7):860–866

    Article  PubMed  CAS  Google Scholar 

  4. Hongo K, Kobayashi S, Okudera H, Hokama M, Nakagawa F (1995) Noninvasive cerebral optical spectroscopy—depth-resolved measurements of cerebral hemodynamics using indocyanine green. Neurolog Res 17(2):89–93

    CAS  Google Scholar 

  5. Towle EL, Richards LM, Shams Kazmi S, Fox DJ, Dunn AK (2012) Comparison of indocyanine green angiography and laser speckle contrast imaging for the assessment of vasculature perfusion. Neurosurgery 71(5):1023–1030; discussion 1030–1021. doi:10.1227/NEU.0b013e31826adf88.

    Google Scholar 

  6. Paul JS, Luft AR, Yew E, Sheu FS (2006) Imaging the development of an ischemic core following photochemically induced cortical infarction in rats using Laser Speckle Contrast Analysis (LASCA). Neuroimage 29(1):38–45. doi:10.1016/j.neuroimage.2005.07.019

    Article  PubMed  Google Scholar 

  7. Dunn AK, Bolay H, Moskowitz MA, Boas DA (2001) Dynamic imaging of cerebral blood flow using laser speckle. J Cereb Blood Flow Metab 21(3):195–201. doi:10.1097/00004647-200103000-00002

    Article  PubMed  CAS  Google Scholar 

  8. Sheth SA, Prakash N, Guiou M, Toga AW (2009) Validation and visualization of two-dimensional optical spectroscopic imaging of cerebral hemodynamics. Neuroimage 47(Suppl 2):T36–T43. doi:10.1016/j.neuroimage.2008.09.060

    Article  PubMed  PubMed Central  Google Scholar 

  9. Prakash N, Uhlemann F, Sheth SA, Bookheimer S, Martin N, Toga AW (2009) Current trends in intraoperative optical imaging for functional brain mapping and delineation of lesions of language cortex. Neuroimage 47(Suppl 2):T116–126. doi:10.1016/j.neuroimage.2008.07.066

    Article  PubMed  PubMed Central  Google Scholar 

  10. Casasent D, Chen XW (2004) Feature reduction and morphological processing for hyperspectral image data. Appl Opt 43(2):227–236

    Article  PubMed  Google Scholar 

  11. Bannon D (2009) Hyperspectral imaging: cubes and slices. Nat Photon 3(11):627–629. doi:10.1038/nphoton.2009.205

    Article  CAS  Google Scholar 

  12. Akbari H, Halig LV, Schuster DM, Osunkoya A, Master V, Nieh PT, Chen GZ, Fei B (2012) Hyperspectral imaging and quantitative analysis for prostate cancer detection. J Biomed Opt 17(7):076005. doi:10.1117/1.JBO.17.7.076005

    Article  PubMed  PubMed Central  Google Scholar 

  13. Goetz AF, Vane G, Solomon JE, Rock BN (1985) Imaging spectrometry for Earth remote sensing. Science 228(4704):1147–1153. doi:10.1126/science.228.4704.1147

    Article  PubMed  CAS  Google Scholar 

  14. Jobsis FF, Keizer JH, LaManna JC, Rosenthal M (1977) Reflectance spectrophotometry of cytochrome aa3 in vivo. J Appl Physiol 43(5):858–872

    PubMed  CAS  Google Scholar 

  15. Sylvia AL, Rosenthal M (1979) Effects of age on brain oxidative metabolism in vivo. Brain Res 165(2):235–248

    Article  PubMed  CAS  Google Scholar 

  16. Wolf T, Lindauer U, Obrig H, Dreier J, Back T, Villringer A, Dirnagl U (1996) Systemic nitric oxide synthase inhibition does not affect brain oxygenation during cortical spreading depression in rats: a noninvasive near-infrared spectroscopy and laser-Doppler flowmetry study. J Cereb Blood Flow Metab 16(6):1100–1107. doi:10.1097/00004647-199611000-00003

    Article  PubMed  CAS  Google Scholar 

  17. Yin C, Zhou F, Wang Y, Luo W, Luo Q, Li P (2013) Simultaneous detection of hemodynamics, mitochondrial metabolism and light scattering changes during cortical spreading depression in rats based on multi-spectral optical imaging. Neuroimage 76:70–80. doi:10.1016/j.neuroimage.2013.02.079

    Article  PubMed  CAS  Google Scholar 

  18. Ellingsen PG, Nystrom S, Reitan NK, Lindgren M (2013) Spectral correlation analysis of amyloid beta plaque inhomogeneity from double staining experiments. J Biomed Opt 18(10):101313. doi:10.1117/1.JBO.18.10.101313

    Article  PubMed  Google Scholar 

  19. Ellingsen PG, Reitan NK, Pedersen BD, Lindgren M (2013) Hyperspectral analysis using the correlation between image and reference. J Biomed Opt 18(2):20501. doi:10.1117/1.JBO.18.2.020501

    Article  PubMed  Google Scholar 

  20. Satori S, Aoyanagi Y, Hara U, Mitsuhashi R, Takeuchi Y (2008) Hyperspectral sensor HSC3000 for nano-satellite ’TAIKI’. 7149:71490M–71490M-71499. doi:10.1117/12.804898.

  21. Zhang HF, Maslov K, Sivaramakrishnan M, Stoica G, Wang LV (2007) Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy. Appl Phys Lett 90(5):053901–053901–053903

    Google Scholar 

  22. Maslov K, Zhang HF, Wang LV (2007) Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculature in vivo. Inverse Prob 23(6):S113

    Article  Google Scholar 

  23. Frostig RD, Lieke EE, Ts’o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci 87(16):6082– 6086

    Google Scholar 

  24. Kashani AH, Kirkman E, Martin G, Humayun MS (2011) Hyperspectral computed tomographic imaging spectroscopy of vascular oxygen gradients in the rabbit retina in vivo. PloS One 6(9): e24482

    Google Scholar 

  25. Subramanian NR, Kerekes JP, Kearney K, Schad N (2006) Spectral imaging of near-surface oxygen saturation. In: Medical imaging, 2006. International Society for Optics and Photonics, pp 61423Y–61423Y–61429

  26. Mirkovic J, Lau C, McGee S, Yu CC, Nazemi J, Galindo L, Feng V, Darragh T, de Las Morenas A, Crum C, Stier E, Feld M, Badizadegan K (2009) Effect of anatomy on spectroscopic detection of cervical dysplasia. J Biomed Opt 14(4):044021. doi:10.1117/1.3194142

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ramella-Roman JC, Mathews SA, Kandimalla H, Nabili A, Duncan DD, D’Anna SA, Shah SM, Nguyen QD (2008) Measurement of oxygen saturation in the retina with a spectroscopic sensitive multi aperture camera. Opt Express 16(9):6170–6182

    Article  PubMed  CAS  Google Scholar 

  28. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR (1997) A rat model of focal embolic cerebral ischemia. Brain Res 766(1–2):83–92

    Article  PubMed  CAS  Google Scholar 

  29. Kiyota Y, Pahlmark K, Memezawa H, Smith ML, Siesjo BK (1993) Free radicals and brain damage due to transient middle cerebral artery occlusion: the effect of dimethylthiourea. Exp Brain Res 95(3):388–396

    Article  PubMed  CAS  Google Scholar 

  30. Li L, Ke Z, Tong KY, Ying M (2010) Evaluation of cerebral blood flow changes in focal cerebral ischemia rats by using transcranial Doppler ultrasonography. Ultrasound Med Biol 36(4):595–603. doi:10.1016/j.ultrasmedbio.2010.01.005

    Article  PubMed  Google Scholar 

  31. Powers WJ, Press GA, Grubb RL Jr, Gado M, Raichle ME (1987) The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Ann Intern Med 106(1):27–34

    Article  PubMed  CAS  Google Scholar 

  32. Baron JC, Bousser MG, Rey A, Guillard A, Comar D, Castaigne P (1981) Reversal of focal “misery-perfusion syndrome” by extra-intracranial arterial bypass in hemodynamic cerebral ischemia. A case study with 15O positron emission tomography. Stroke; J Cereb Circul 12(4):454–459

    Article  CAS  Google Scholar 

  33. Awano T, Sakatani K, Yokose N, Kondo Y, Igarashi T, Hoshino T, Nakamura S, Fujiwara N, Murata Y, Katayama Y, Shikayama T, Miwa M (2010) Intraoperative EC-IC bypass blood flow assessment with indocyanine green angiography in moyamoya and non-moyamoya ischemic stroke. World Neurosurg 73(6):668–674. doi:10.1016/j.wneu.2010.03.027

    Article  PubMed  Google Scholar 

  34. Nakagawa A, Fujimura M, Arafune T, Sakuma I, Tominaga T (2009) Clinical implications of intraoperative infrared brain surface monitoring during superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. J Neurosurg 111(6):1158–1164. doi:10.3171/2009.4.JNS08585

    Article  PubMed  Google Scholar 

  35. Hoshino T, Katayama Y, Sakatani K, Kano T, Murata Y (2006) Intraoperative monitoring of cerebral blood oxygenation and hemodynamics during extracranial-intracranial bypass surgery by a newly developed visible light spectroscopy system. Surg Neurol 65(6):569–576; discussion 576. doi:10.1016/j.surneu.2005.09.028

  36. Sun X, Wang Y, Chen S, Luo W, Li P, Luo Q (2011) Simultaneous monitoring of intracellular pH changes and hemodynamic response during cortical spreading depression by fluorescence-corrected multimodal optical imaging. Neuroimage 57(3):873–884. doi:10.1016/j.neuroimage.2011.05.040

    Google Scholar 

  37. Dunn AK, Devor A, Bolay H, Andermann ML, Moskowitz MA, Dale AM, Boas DA (2003) Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. Opt Lett 28(1):28–30

    Article  PubMed  CAS  Google Scholar 

  38. Eggert HR, Blazek V (1987) Optical properties of human brain tissue, meninges, and brain tumors in the spectral range of 200 to 900 nm. Neurosurgery 21(4):459–464

    Article  PubMed  CAS  Google Scholar 

  39. Hochman DW (2000) Optical monitoring of neuronal activity: brain-mapping on a shoestring. Brain Cogn 42(1):56–59. doi:10.1006/brcg.1999.1161

    Article  PubMed  CAS  Google Scholar 

  40. Haglund MM, Ojemann GA, Hochman DW (1992) Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 358(6388):668–671. doi:10.1038/358668a0

    Google Scholar 

  41. Toms SA, Lin WC, Weil RJ, Johnson MD, Jansen ED, Mahadevan-Jansen A (2007) Intraoperative optical spectroscopy identifies infiltrating glioma margins with high sensitivity. Neurosurgery 61(1 Suppl):327–335; discussion 335–326. doi:10.1227/01.neu.0000279226.68751.21

    Google Scholar 

  42. Lin WC, Sandberg DI, Bhatia S, Johnson M, Morrison G, Ragheb J (2009) Optical spectroscopy for in-vitro differentiation of pediatric neoplastic and epileptogenic brain lesions. J Biomed Opt 14(1):014028. doi:10.1117/1.3080144

    Google Scholar 

  43. Kayama T, Yoshimoto T, Fujimoto S, Sakurai Y (1991) Intratumoral oxygen pressure in malignant brain tumor. J Neurosurg 74(1):55–59. doi:10.3171/jns.1991.74.1.0055

    Article  PubMed  CAS  Google Scholar 

  44. Jensen RL (2009) Brain tumor hypoxia: tumorigenesis, angiogenesis, imaging, pseudoprogression, and as a therapeutic target. J Neuro-Oncol 92(3):317–335. doi:10.1007/s11060-009-9827-2

    Article  CAS  Google Scholar 

  45. Graf BW, Ralston TS, Ko HJ, Boppart SA (2009) Detecting intrinsic scattering changes correlated to neuron action potentials using optical coherence imaging. Opt Express 17(16):13447–13457

    Article  PubMed  PubMed Central  Google Scholar 

  46. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ (1998) Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 42(3):518–525; discussion 525–516

    Google Scholar 

  47. Valdes PA, Leblond F, Jacobs VL, Wilson BC, Paulsen KD, Roberts DW (2012) Quantitative, spectrally-resolved intraoperative fluorescence imaging. Sci Rep 2:798. doi:10.1038/srep00798

    Article  PubMed  PubMed Central  Google Scholar 

  48. Valdes PA, Kim A, Leblond F, Conde OM, Harris BT, Paulsen KD, Wilson BC, Roberts DW (2011) Combined fluorescence and reflectance spectroscopy for in vivo quantification of cancer biomarkers in low- and high-grade glioma surgery. J Biomed Opt 16(11):116007. doi:10.1117/1.3646916

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Junji Kishimoto for his valuable assistance with the statistical analyses.

Conflict of interest

The authors declare no conflict of interest in association with this study.

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Authors and Affiliations

  1. Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Megumu Mori, Akira Nakamizo, Yuichiro Kikkawa, Koji Yoshimoto, Masahiro Mizoguchi & Tomio Sasaki

  2. PENTAX Lifecare Division Medical Instrument SBU, HOYA Corporation, 1-1-110 Tsutsujigaoka, Akishima-shi, Tokyo, 196-0012, Japan

    Toru Chiba

  3. Department of Advanced Medicine and Innovative Technology, Kyushu University Hospital, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Ryuichi Kumashiro & Morimasa Tomikawa

  4. Innovation Center for Medical Redox Navigation, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Masaharu Murata

  5. Department of Advanced Medical Initiatives, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Tomohiko Akahoshi & Makoto Hashizume

Authors
  1. Megumu Mori
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  2. Toru Chiba
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  3. Akira Nakamizo
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  4. Ryuichi Kumashiro
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  11. Tomio Sasaki
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  12. Makoto Hashizume
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Correspondence to Makoto Hashizume.

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Mori, M., Chiba, T., Nakamizo, A. et al. Intraoperative visualization of cerebral oxygenation using hyperspectral image data: a two-dimensional mapping method. Int J CARS 9, 1059–1072 (2014). https://doi.org/10.1007/s11548-014-0989-9

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  • DOI: https://doi.org/10.1007/s11548-014-0989-9

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