Abstract

Noninvasive monitoring of cerebral blood oxygenation with an optoacoustic technique offers advantages over current invasive and noninvasive methods. We report the results of in vivo studies in the sheep superior sagittal sinus (SSS), a large central cerebral vein. We changed blood oxygenation by increasing and decreasing the inspired fraction of oxygen (FiO2). Optoacoustic measurements from the SSS were performed at wavelengths of 700, 800, and 1064 nm using an optical parametric oscillator as a source of pulsed near-infrared light. Actual oxygenation of SSS blood was measured with a CO-Oximeter in blood samples drawn from the SSS through a small craniotomy. The amplitude of the optoacoustic signal induced in the SSS blood at λ = 1064 nm closely followed the changes in blood oxygenation, at λ = 800 nm was almost constant, and at λ = 700 nm was changing in the opposite direction, all in accordance with the absorption spectra of oxy- and deoxyhemoglobin. The optoacoustically predicted oxygenation correlated well with actual blood oxygenation in sheep SSS (R 2 = 0.965 to 0.990). The accuracy was excellent, with a mean difference of 4.8% to 9.3% and a standard deviation of 2.8% to 4.2%. To the best of our knowledge, this paper reports for the first time accurate measurements of cerebral venous blood oxygenation validated against the “gold standard” CO-Oximetry method.

© 2009 Optical Society of America

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2007

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2005

Y. Y. Petrov, D. S. Prough, D. E. Deyo, M. Klasing, M. Motamedi, and R. O. Esenaliev, "Optoacoustic, noninvasive, real-time, continuous monitoring of cerebral blood oxygenation: an in vivo study in sheep," Anesthesiology 102, 69-75 (2005).
[CrossRef]

2004

J. M. Murkin, "Perioperative detection of brain oxygenation and clinical outcomes in cardiac surgery," Semin. Cardiothorac. Vasc. Anesth. 8, 13-14 (2004).
[CrossRef] [PubMed]

W. J. Stevens, "Multimodal monitoring: head injury management using SjvO2 and LICOX," J. Neurosci. Nurs. 36, 332-339 (2004).
[CrossRef]

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

2003

M. Soehle, M. Jaeger, and J. Meixensberger, "Online assessment of brain tissue oxygen autoregulation in traumatic brain injury and subarachnoid hemorrhage," Neurol. Res. 25, 411-417 (2003).
[CrossRef] [PubMed]

2002

1998

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

C. R. Simpson, M. Kohl, M. Essenpreis, and M. Cope, "Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique," Phys. Med. Biol. 43, 2465-2478 (1998).
[CrossRef] [PubMed]

1990

W. - F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron. 26, 2166-2185 (1990).
[CrossRef]

1977

F. F. Jobsis, "Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters," Science 198, 1264-1267 (1977).
[CrossRef] [PubMed]

1973

1943

B. L. Horecker, "The absorption spectra of hemoglobin and its derivatives in the visible and near infra-red regions," J. Biol. Chem. 148, 173-183 (1943).

Bien, T.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Brawanski, A.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Brecht, H. P.

Cheong, W. - F.

W. - F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron. 26, 2166-2185 (1990).
[CrossRef]

Choi, J. H.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Cicenaite, I.

Comelli, D.

Cope, M.

C. R. Simpson, M. Kohl, M. Essenpreis, and M. Cope, "Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique," Phys. Med. Biol. 43, 2465-2478 (1998).
[CrossRef] [PubMed]

Deyo, D. E.

Y. Y. Petrov, D. S. Prough, D. E. Deyo, M. Klasing, M. Motamedi, and R. O. Esenaliev, "Optoacoustic, noninvasive, real-time, continuous monitoring of cerebral blood oxygenation: an in vivo study in sheep," Anesthesiology 102, 69-75 (2005).
[CrossRef]

R. O. Esenaliev, I. V. Larina, K. V. Larin, D. E. Deyo, M. Motamedi, and D. S. Prough, "Optoacoustic technique for noninvasive monitoring of blood oxygenation: a feasibility study," Appl. Opt. 41, 4722-4731 (2002).
[CrossRef] [PubMed]

Deyo, D. J.

Esenaliev, R. O.

Essenpreis, M.

C. R. Simpson, M. Kohl, M. Essenpreis, and M. Cope, "Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique," Phys. Med. Biol. 43, 2465-2478 (1998).
[CrossRef] [PubMed]

Farina, A.

Gratton, E.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Gupta, R.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Hale, G. M.

Holzschuh, M.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Horecker, B. L.

B. L. Horecker, "The absorption spectra of hemoglobin and its derivatives in the visible and near infra-red regions," J. Biol. Chem. 148, 173-183 (1943).

Hueber, D.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Jaeger, M.

M. Soehle, M. Jaeger, and J. Meixensberger, "Online assessment of brain tissue oxygen autoregulation in traumatic brain injury and subarachnoid hemorrhage," Neurol. Res. 25, 411-417 (2003).
[CrossRef] [PubMed]

Jobsis, F. F.

F. F. Jobsis, "Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters," Science 198, 1264-1267 (1977).
[CrossRef] [PubMed]

Kallenbach, B.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Kienle, A.

Klasing, M.

Y. Y. Petrov, D. S. Prough, D. E. Deyo, M. Klasing, M. Motamedi, and R. O. Esenaliev, "Optoacoustic, noninvasive, real-time, continuous monitoring of cerebral blood oxygenation: an in vivo study in sheep," Anesthesiology 102, 69-75 (2005).
[CrossRef]

Kohl, M.

C. R. Simpson, M. Kohl, M. Essenpreis, and M. Cope, "Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique," Phys. Med. Biol. 43, 2465-2478 (1998).
[CrossRef] [PubMed]

Ku, G.

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography," J. Biomed. Opt. 11, 024015 (9 pages).
[PubMed]

Larin, K. V.

Larina, I. V.

Mantulin, W.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Meixensberger, J.

M. Soehle, M. Jaeger, and J. Meixensberger, "Online assessment of brain tissue oxygen autoregulation in traumatic brain injury and subarachnoid hemorrhage," Neurol. Res. 25, 411-417 (2003).
[CrossRef] [PubMed]

Metz, C.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Michalos, A.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Motamedi, M.

Y. Y. Petrov, D. S. Prough, D. E. Deyo, M. Klasing, M. Motamedi, and R. O. Esenaliev, "Optoacoustic, noninvasive, real-time, continuous monitoring of cerebral blood oxygenation: an in vivo study in sheep," Anesthesiology 102, 69-75 (2005).
[CrossRef]

R. O. Esenaliev, I. V. Larina, K. V. Larin, D. E. Deyo, M. Motamedi, and D. S. Prough, "Optoacoustic technique for noninvasive monitoring of blood oxygenation: a feasibility study," Appl. Opt. 41, 4722-4731 (2002).
[CrossRef] [PubMed]

Murkin, J. M.

J. M. Murkin, "Perioperative detection of brain oxygenation and clinical outcomes in cardiac surgery," Semin. Cardiothorac. Vasc. Anesth. 8, 13-14 (2004).
[CrossRef] [PubMed]

Oraevsky, A. A.

G. M. Spirou, A. A. Oraevsky, I. A. Vitkin, and W. M. Whelan, "Optical and acoustical properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics," Phys. Med. Biol. 50, N141-N153 (2005).
[PubMed]

Patrikeev, I.

Petrov, Y. Y.

Petrova, I. Y.

Pifferi, A.

Polzonetti, C.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Prahl, S. A.

W. - F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron. 26, 2166-2185 (1990).
[CrossRef]

Prough, D. S.

Querry, M. R.

Rothoerl, R.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Safonova, L. P.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Simpson, C. R.

C. R. Simpson, M. Kohl, M. Essenpreis, and M. Cope, "Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique," Phys. Med. Biol. 43, 2465-2478 (1998).
[CrossRef] [PubMed]

Soehle, M.

M. Soehle, M. Jaeger, and J. Meixensberger, "Online assessment of brain tissue oxygen autoregulation in traumatic brain injury and subarachnoid hemorrhage," Neurol. Res. 25, 411-417 (2003).
[CrossRef] [PubMed]

Spirou, G. M.

G. M. Spirou, A. A. Oraevsky, I. A. Vitkin, and W. M. Whelan, "Optical and acoustical properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics," Phys. Med. Biol. 50, N141-N153 (2005).
[PubMed]

Stevens, W. J.

W. J. Stevens, "Multimodal monitoring: head injury management using SjvO2 and LICOX," J. Neurosci. Nurs. 36, 332-339 (2004).
[CrossRef]

Stoica, G.

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography," J. Biomed. Opt. 11, 024015 (9 pages).
[PubMed]

Taeger, K.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Taroni, P.

Toronov, V.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Vitkin, I. A.

G. M. Spirou, A. A. Oraevsky, I. A. Vitkin, and W. M. Whelan, "Optical and acoustical properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics," Phys. Med. Biol. 50, N141-N153 (2005).
[PubMed]

Wang, L. V.

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography," J. Biomed. Opt. 11, 024015 (9 pages).
[PubMed]

Wang, X.

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography," J. Biomed. Opt. 11, 024015 (9 pages).
[PubMed]

Welch, A. J.

W. - F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron. 26, 2166-2185 (1990).
[CrossRef]

Whelan, W. M.

G. M. Spirou, A. A. Oraevsky, I. A. Vitkin, and W. M. Whelan, "Optical and acoustical properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics," Phys. Med. Biol. 50, N141-N153 (2005).
[PubMed]

Woertgen, C.

C. Metz, M. Holzschuh, T. Bien, C. Woertgen, R. Rothoerl, B. Kallenbach, K. Taeger, and A. Brawanski, "Monitoring of cerebral oxygen metabolism in the jugular bulb: reliability of unilateral measurements in severe head injury," J. Cereb. Blood Flow Metab. 18, 332-343 (1998).
[CrossRef] [PubMed]

Wolf, M.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Wolf, U.

J. H. Choi, M. Wolf, V. Toronov, U. Wolf, C. Polzonetti, D. Hueber, L. P. Safonova, R. Gupta, A. Michalos, W. Mantulin, and E. Gratton, "Noninvasive determination of the optical properties of adult brain: near-infrared spectroscopy approach," J. Biomed. Opt. 9, 221-229 (2004).
[CrossRef] [PubMed]

Xie, X.

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography," J. Biomed. Opt. 11, 024015 (9 pages).
[PubMed]

Anesthesiology

Y. Y. Petrov, D. S. Prough, D. E. Deyo, M. Klasing, M. Motamedi, and R. O. Esenaliev, "Optoacoustic, noninvasive, real-time, continuous monitoring of cerebral blood oxygenation: an in vivo study in sheep," Anesthesiology 102, 69-75 (2005).
[CrossRef]

Appl. Opt.

IEEE J. Quantum Electron.

W. - F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron. 26, 2166-2185 (1990).
[CrossRef]

J. Biol. Chem.

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Figures (9)

Fig. 1.
Fig. 1.

Schematic diagram of the optoacoustic probe.

Fig. 2.
Fig. 2.

Optoacoustic signals recorded from the SSS phantom with blood at different oxygenation at the wavelengths of 700 nm (a) and 1064 nm (b).

Fig. 3.
Fig. 3.

(a) Optoacoustic signal amplitudes at 700 nm and 1064 nm normalized by the amplitude at 805 nm. (b) Calibration curve obtained by dividing the fitting line for 1064 nm by the fitting line for 700 nm in (a).

Fig. 4.
Fig. 4.

Optoacoustic signals from sheep skull over the SSS at wavelengths of 700 nm (a), 800 nm (b), and 1064 nm (c) for different levels of blood oxygenation.

Fig. 5.
Fig. 5.

Directly measured SSS blood oxygenation (black, both a and b) and normalized optoacoustic signal amplitude at 700 nm (blue, a) and 1064 nm (red, b) during 2 cycles of changes in blood oxygenation.

Fig. 6.
Fig. 6.

Optoacoustic signal amplitudes measured from the sheep SSS in vivo at 700 nm (blue triangles) and 1064 nm (red circles) corrected by the change in the amplitude at 805 nm. The linear fit to the data is presented as well.

Fig. 7.
Fig. 7.

(a) Correlation between optoacoustically predicted and actual SSS blood oxygenation during two cycles of changes in blood oxygenation. (b) Standard deviation and bias of the difference between predicted and actual oxygenation.

Fig. 8.
Fig. 8.

SSS blood oxygenation (black, both a and b) and normalized optoacoustic signal amplitude at 700 nm (blue, a) and 1064 nm (red, b) measured in a sheep with low motion artifacts.

Fig. 9.
Fig. 9.

(a) Correlation between optoacoustically predicted and actual SSS blood oxygenation for the measurement with low motion artifacts. (b) Standard deviation and bias of the difference between predicted and actual oxygenation.

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