Abstract

Deterioration in mitochondrial function leads to hepatic ischemia and reperfusion injury (IRI) in liver surgery and transplantation. 3D optical cryoimaging was used to measure the levels of mitochondrial coenzymes NADH and FAD, and their redox ratio (NADH/FAD) gave a quantitative marker for hepatocyte oxidative stress during IRI. Using a rat model, five groups were compared: control, ischemia for 60 or 90 minutes (Isc60, Isc90), ischemia for 60 or 90 minutes followed by reperfusion of 24 hours (IRI60, IRI90). Ischemia alone did not cause a significant increase in the redox ratio; however, the redox ratio in both IRI60 and IRI90 groups was significantly decreased by 29% and 71%, respectively. A significant correlation was observed between the redox ratio and other markers of injury such as serum aminotransferase levels and the tissue ATP level. The mitochondrial redox state can be successfully measured using optical cryoimaging as a quantitative marker of hepatic IR injury.

© 2017 Optical Society of America

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    [Crossref] [PubMed]

2016 (2)

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

2015 (2)

S.-M. Jeong, “Postreperfusion syndrome during liver transplantation,” Korean J. Anesthesiol. 68(6), 527–539 (2015).
[Crossref] [PubMed]

K. M. Quesnelle, P. V. Bystrom, and L. H. Toledo-Pereyra, “Molecular responses to ischemia and reperfusion in the liver,” Arch. Toxicol. 89(5), 651–657 (2015).
[Crossref] [PubMed]

2014 (1)

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

2012 (2)

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

2011 (1)

A. K. Camara, M. Bienengraeber, and D. F. Stowe, “Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury,” Front. Physiol. 2, 13 (2011).
[Crossref] [PubMed]

2010 (1)

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

2008 (1)

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

2006 (1)

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

2005 (1)

2002 (1)

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

1984 (1)

E. M. Nuutinen, “Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart,” Basic Res. Cardiol. 79(1), 49–58 (1984).
[Crossref] [PubMed]

1979 (2)

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

1962 (1)

R. W. Estabrook, “Fluorometric measurement of reduced pyridine nucleotide in cellular and subcellular particles,” Anal. Biochem. 4(3), 231–245 (1962).
[Crossref] [PubMed]

Abu-Amara, M.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Aguirre, D. A.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Antholine, W. E.

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

Audi, S.

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Austin, G.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Avruch, J. H.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Barlow, C. H.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Bienengraeber, M.

A. K. Camara, M. Bienengraeber, and D. F. Stowe, “Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury,” Front. Physiol. 2, 13 (2011).
[Crossref] [PubMed]

Bruinsma, B. G.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Bystrom, P. V.

K. M. Quesnelle, P. V. Bystrom, and L. H. Toledo-Pereyra, “Molecular responses to ischemia and reperfusion in the liver,” Arch. Toxicol. 89(5), 651–657 (2015).
[Crossref] [PubMed]

Camara, A. K.

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

A. K. Camara, M. Bienengraeber, and D. F. Stowe, “Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury,” Front. Physiol. 2, 13 (2011).
[Crossref] [PubMed]

Camara, A. K. S.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

Casola, G.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Chance, B.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Chang, W.-T.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Cho, H.-D.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Damian, D.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Dash, R. K.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

Davidson, B.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Davidson, B. R.

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

Delpy, D. T.

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

Demos, S. G.

El-Desoky, H.

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

Estabrook, R. W.

R. W. Estabrook, “Fluorometric measurement of reduced pyridine nucleotide in cellular and subcellular particles,” Anal. Biochem. 4(3), 231–245 (1962).
[Crossref] [PubMed]

Fitzgerald, J. T.

Fuller, B.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Gadicherla, A. K.

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

Geerts, S.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Gligor, S.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Hamer, O. W.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Harden, W. R.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Harken, A. H.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Haselgrove, J. C.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Heger, M.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Heisner, J. S.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

Hilmi, I.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Horton, C. N.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Itshak, F.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Jacobs, E. R.

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Jeong, S.-M.

S.-M. Jeong, “Postreperfusion syndrome during liver transplantation,” Korean J. Anesthesiol. 68(6), 527–539 (2015).
[Crossref] [PubMed]

Lavine, J. E.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Liau, I.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Lu, H.-H.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Luo, T.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Maleki, S.

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Marcos, A.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Markmann, J. F.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Martins, P. N.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Michalopoulou, A. P.

Motlagh, M. M.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

Nakase, Y.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Nicolau-Raducu, R.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Nuutinen, E. M.

E. M. Nuutinen, “Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart,” Basic Res. Cardiol. 79(1), 49–58 (1984).
[Crossref] [PubMed]

O’Connor, M.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Oshino, R.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Özer, S.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Planinsic, R. M.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Porte, R. J.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Quesnelle, K. M.

K. M. Quesnelle, P. V. Bystrom, and L. H. Toledo-Pereyra, “Molecular responses to ischemia and reperfusion in the liver,” Arch. Toxicol. 89(5), 651–657 (2015).
[Crossref] [PubMed]

Ranji, M.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Saeidi, N.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Sakai, T.

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

Salehpour, F.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

Schoener, B.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Seifalian, A.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Seifalian, A. M.

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

Sepehr, R.

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Simson, M. B.

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Sirlin, C. B.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Sridharan, G. V.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Staniszewski, K.

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Stowe, D. F.

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

A. K. Camara, M. Bienengraeber, and D. F. Stowe, “Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury,” Front. Physiol. 2, 13 (2011).
[Crossref] [PubMed]

Tapuria, N.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Toledo-Pereyra, L. H.

K. M. Quesnelle, P. V. Bystrom, and L. H. Toledo-Pereyra, “Molecular responses to ischemia and reperfusion in the liver,” Arch. Toxicol. 89(5), 651–657 (2015).
[Crossref] [PubMed]

Troppmann, C.

Uygun, K.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

van Gulik, T. M.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Weeder, P. D.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Woenckhaus, M.

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Wu, Y.-M.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Yang, M.

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

Yang, S. Y.

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Yang, Y.-C.

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Yeh, H.

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Anal. Biochem. (1)

R. W. Estabrook, “Fluorometric measurement of reduced pyridine nucleotide in cellular and subcellular particles,” Anal. Biochem. 4(3), 231–245 (1962).
[Crossref] [PubMed]

Anal. Chem. (1)

H.-H. Lu, Y.-M. Wu, W.-T. Chang, T. Luo, Y.-C. Yang, H.-D. Cho, and I. Liau, “Molecular imaging of ischemia and reperfusion in vivo with mitochondrial autofluorescence,” Anal. Chem. 86(10), 5024–5031 (2014).
[Crossref] [PubMed]

Appl. Opt. (1)

Arch. Toxicol. (1)

K. M. Quesnelle, P. V. Bystrom, and L. H. Toledo-Pereyra, “Molecular responses to ischemia and reperfusion in the liver,” Arch. Toxicol. 89(5), 651–657 (2015).
[Crossref] [PubMed]

Basic Res. Cardiol. (1)

E. M. Nuutinen, “Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart,” Basic Res. Cardiol. 79(1), 49–58 (1984).
[Crossref] [PubMed]

Biochimica et Biophysica Acta (BBA)-Bioenergetics (1)

A. K. Gadicherla, D. F. Stowe, W. E. Antholine, M. Yang, and A. K. Camara, “Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine,” Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817(3), 419–429 (2012).
[Crossref]

Clin. Sci. (1)

A. M. Seifalian, H. El-Desoky, D. T. Delpy, and B. R. Davidson, “Effects of hepatic ischaemia/reperfusion injury in a rabbit model of Indocyanine green clearance,” Clin. Sci. 102(5), 579–586 (2002).
[Crossref] [PubMed]

Crit. Care Med. (1)

C. H. Barlow, W. R. Harden, A. H. Harken, M. B. Simson, J. C. Haselgrove, B. Chance, M. O’Connor, and G. Austin, “Fluorescence mapping of mitochondrial redox changes in heart and brain,” Crit. Care Med. 7(9), 402–406 (1979).
[Crossref] [PubMed]

Front. Physiol. (1)

A. K. Camara, M. Bienengraeber, and D. F. Stowe, “Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury,” Front. Physiol. 2, 13 (2011).
[Crossref] [PubMed]

IEEE J. Transl. Eng. Health Med. (1)

M. Ranji, M. M. Motlagh, F. Salehpour, R. Sepehr, J. S. Heisner, R. K. Dash, and A. K. S. Camara, “Optical Cryoimaging Reveals a Heterogeneous Distribution of Mitochondrial Redox State in ex vivo Guinea Pig Hearts and Its Alteration During Ischemia and Reperfusion,” IEEE J. Transl. Eng. Health Med. 4, 1800210 (2016).
[PubMed]

J. Biol. Chem. (1)

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

J. Biomed. Opt. (1)

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Korean J. Anesthesiol. (1)

S.-M. Jeong, “Postreperfusion syndrome during liver transplantation,” Korean J. Anesthesiol. 68(6), 527–539 (2015).
[Crossref] [PubMed]

Liver Transpl. (2)

I. Hilmi, C. N. Horton, R. M. Planinsic, T. Sakai, R. Nicolau-Raducu, D. Damian, S. Gligor, and A. Marcos, “The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation,” Liver Transpl. 14(4), 504–508 (2008).
[Crossref] [PubMed]

M. Abu-Amara, S. Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian, “Liver ischemia/reperfusion injury: processes in inflammatory networks-a review,” Liver Transpl. 16(9), 1016–1032 (2010).
[Crossref] [PubMed]

Radiographics (1)

O. W. Hamer, D. A. Aguirre, G. Casola, J. E. Lavine, M. Woenckhaus, and C. B. Sirlin, “Fatty liver: Imaging patterns and pitfalls 1,” Radiographics 26(6), 1637–1653 (2006).
[Crossref] [PubMed]

Sci. Rep. (1)

B. G. Bruinsma, G. V. Sridharan, P. D. Weeder, J. H. Avruch, N. Saeidi, S. Özer, S. Geerts, R. J. Porte, M. Heger, T. M. van Gulik, P. N. Martins, J. F. Markmann, H. Yeh, and K. Uygun, “Metabolic profiling during ex vivo machine perfusion of the human liver,” Sci. Rep. 6(1), 22415 (2016).
[Crossref] [PubMed]

Other (2)

C. García-Ruíz, A. Morales, and J. C. Fernández-Checa, “Oxidative Stress and Liver Ischemia–Reperfusion Injury,” in Studies on Hepatic Disorders, 149–170 (2015).

T. Vo-Dinh, Biomedical Photonics Handbook: Therapeutics and Advanced Biophotonics (CRC press, 2014).

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Figures (5)

Fig. 1
Fig. 1

Sample images of livers for each treatment: a) control (Ctrl), b) ischemia for 60 or 90 minutes (Isc) by blocking the blood flow with a clamp (as shown with the red circle) c) 24h reperfusion after ischemia (IRI).

Fig. 2
Fig. 2

a) Maximum projection of the redox ratio for n = 5 samples in each group. Each image scale is 4 cm × 4 cm. b) Relative voxel frequency distribution of redox ratio for a representative sample in each group.

Fig. 3
Fig. 3

Statistical analysis of mean values of RR with n = 5 samples in each group and significant difference marked with *.

Fig. 4
Fig. 4

Correlation of mean RR with a) AST, b) ALT, and c) ATP measurements from fifteen animals in control, IRI60, and IRI90 groups. RR had a significant negative correlation with serum liver enzyme levels (AST and ALT), and a significant positive correlation with tissue ATP levels. These results imply that RR decreases as a hepatocyte injury progresses.

Fig. 5
Fig. 5

3D rendering of redox ratio for a representative sample in each group.

Tables (1)

Tables Icon

Table 1 Overview of AST, ALT, and ATP measurements for each sample group. Stars show a significant difference (p < 0.05) from the control group. Unit of AST and ALT is enzyme unit/L (U/L) and for ATP it is Luminescence/g.

Equations (2)

Equations on this page are rendered with MathJax. Learn more.

Redox Ratio = NADH/ FAD ,
Redox Ratio Mean (RR) = 1 N i=1 N Liver_Volume(i) ,

Metrics