Abstract

Few technologies are capable of imaging in vivo function during development. In this study, we have implemented spectral photoacoustic imaging to estimate tissue oxygenation longitudinally in pregnant mice. We used the spectral photoacoustic signal to estimate hemoglobin oxygen saturation within intact, in vivo mouse concepti from developmental day (E) 8.5 to E16.5—a first step towards functional imaging of the maternal-fetal environment. Future work will apply these methods to compare longitudinal functional changes during normal vs abnormal development of embryos, fetuses, and placentas.

© 2017 Optical Society of America

Full Article  |  PDF Article
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    [Crossref] [PubMed]
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2016 (4)

J. Weber, P. C. Beard, and S. E. Bohndiek, “Contrast agents for molecular photoacoustic imaging,” Nat. Methods 13(8), 639–650 (2016).
[Crossref] [PubMed]

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

A. D. Yzaguirre and N. A. Speck, “Extravascular endothelial and hematopoietic islands form through multiple pathways in midgestation mouse embryos,” Dev. Biol. 415(1), 111–121 (2016).
[Crossref] [PubMed]

2015 (3)

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

G. P. Luke and S. Y. Emelianov, “Label-free Detection of Lymph Node Metastases with US-guided Functional Photoacoustic Imaging,” Radiology 277(2), 435–442 (2015).
[Crossref] [PubMed]

2014 (2)

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

2013 (5)

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

J. O. Lo, J. F. Mission, and A. B. Caughey, “Hypertensive disease of pregnancy and maternal mortality,” Curr. Opin. Obstet. Gynecol. 25(2), 124–132 (2013).
[Crossref] [PubMed]

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref] [PubMed]

2012 (5)

C. L. Bayer, G. P. Luke, and S. Y. Emelianov, “Photoacoustic imaging for medical diagnostics,” Acoust. Today 8(4), 15–23 (2012).
[Crossref] [PubMed]

S. Bake, J. D. Tingling, and R. C. Miranda, “Ethanol exposure during pregnancy persistently attenuates cranially directed blood flow in the developing fetus: evidence from ultrasound imaging in a murine second trimester equivalent model,” Alcohol. Clin. Exp. Res. 36(5), 748–758 (2012).
[Crossref] [PubMed]

G. P. Luke, D. Yeager, and S. Y. Emelianov, “Biomedical applications of photoacoustic imaging with exogenous contrast agents,” Ann. Biomed. Eng. 40(2), 422–437 (2012).
[Crossref] [PubMed]

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17(6), 061202 (2012).
[Crossref] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

2011 (1)

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

2009 (1)

E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref] [PubMed]

2008 (1)

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

2007 (1)

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

2006 (1)

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

2004 (1)

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

2003 (2)

L. Leatherbury, Q. Yu, and C. W. Lo, “Noninvasive phenotypic analysis of cardiovascular structure and function in fetal mice using ultrasound,” Birth Defects Res. C Embryo Today 69(1), 83–91 (2003).
[Crossref] [PubMed]

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

1979 (1)

J. W. Severinghaus, “Simple, accurate equations for human blood O2 dissociation computations,” J. Appl. Physiol. 46(3), 599–602 (1979).
[PubMed]

1958 (1)

J. W. Severinghaus, “Oxyhemoglobin dissociation curve correction for temperature and pH variation in human blood,” J. Appl. Physiol. 12(3), 485–486 (1958).
[PubMed]

Adam, D.

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

Adamson, S. L.

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

Albanese, S.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Aristizábal, O.

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Armit, C.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Arnal, B.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Arridge, S. R.

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17(6), 061202 (2012).
[Crossref] [PubMed]

Bake, S.

S. Bake, J. D. Tingling, and R. C. Miranda, “Ethanol exposure during pregnancy persistently attenuates cranially directed blood flow in the developing fetus: evidence from ultrasound imaging in a murine second trimester equivalent model,” Alcohol. Clin. Exp. Res. 36(5), 748–758 (2012).
[Crossref] [PubMed]

Baldock, R. A.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Baldwin, H. S.

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Barash, J.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Bar-Zion, A.

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

Bayer, C. L.

C. L. Bayer, G. P. Luke, and S. Y. Emelianov, “Photoacoustic imaging for medical diagnostics,” Acoust. Today 8(4), 15–23 (2012).
[Crossref] [PubMed]

Beard, P.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Beard, P. C.

J. Weber, P. C. Beard, and S. E. Bohndiek, “Contrast agents for molecular photoacoustic imaging,” Nat. Methods 13(8), 639–650 (2016).
[Crossref] [PubMed]

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17(6), 061202 (2012).
[Crossref] [PubMed]

Bentley, T.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Bohndiek, S. E.

J. Weber, P. C. Beard, and S. E. Bohndiek, “Contrast agents for molecular photoacoustic imaging,” Nat. Methods 13(8), 639–650 (2016).
[Crossref] [PubMed]

Brown, S. D.

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Brunetti, A.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Bunger, R.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Burton, N.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Cahill, L. S.

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

Caughey, A. B.

J. O. Lo, J. F. Mission, and A. B. Caughey, “Hypertensive disease of pregnancy and maternal mortality,” Curr. Opin. Obstet. Gynecol. 25(2), 124–132 (2013).
[Crossref] [PubMed]

Cleary, J.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Coda, A. R. D.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Cox, B.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17(6), 061202 (2012).
[Crossref] [PubMed]

Cullen, J. M.

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

Delpy, D.

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Duhm, J.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Dunning, P. S.

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Elmore, S. A.

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

Elwell, C.

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Emelianov, S. Y.

G. P. Luke and S. Y. Emelianov, “Label-free Detection of Lymph Node Metastases with US-guided Functional Photoacoustic Imaging,” Radiology 277(2), 435–442 (2015).
[Crossref] [PubMed]

G. P. Luke, D. Yeager, and S. Y. Emelianov, “Biomedical applications of photoacoustic imaging with exogenous contrast agents,” Ann. Biomed. Eng. 40(2), 422–437 (2012).
[Crossref] [PubMed]

C. L. Bayer, G. P. Luke, and S. Y. Emelianov, “Photoacoustic imaging for medical diagnostics,” Acoust. Today 8(4), 15–23 (2012).
[Crossref] [PubMed]

Foley, J. F.

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

Fontana, J. L.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Foster, F. S.

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

Gargiulo, S.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Gonzalez-Bulnes, A.

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

Graham, L.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Gramanzini, M.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Greco, A.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Greene, N. D. E.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Hasan, T.

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

Henkelman, R. M.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Hill, B.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Hurley, R. J.

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Jacques, S. L.

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref] [PubMed]

Ji, R. P.

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Johnson, P.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Ketterling, J. A.

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

Laufer, J.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Laufer, J. G.

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17(6), 061202 (2012).
[Crossref] [PubMed]

Leatherbury, L.

L. Leatherbury, Q. Yu, and C. W. Lo, “Noninvasive phenotypic analysis of cardiovascular structure and function in fetal mice using ultrasound,” Birth Defects Res. C Embryo Today 69(1), 83–91 (2003).
[Crossref] [PubMed]

Liuzzi, R.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Livingston, D. P.

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

Lo, C. W.

L. Leatherbury, Q. Yu, and C. W. Lo, “Noninvasive phenotypic analysis of cardiovascular structure and function in fetal mice using ultrasound,” Birth Defects Res. C Embryo Today 69(1), 83–91 (2003).
[Crossref] [PubMed]

Lo, J. O.

J. O. Lo, J. F. Mission, and A. B. Caughey, “Hypertensive disease of pregnancy and maternal mortality,” Curr. Opin. Obstet. Gynecol. 25(2), 124–132 (2013).
[Crossref] [PubMed]

Luke, G. P.

G. P. Luke and S. Y. Emelianov, “Label-free Detection of Lymph Node Metastases with US-guided Functional Photoacoustic Imaging,” Radiology 277(2), 435–442 (2015).
[Crossref] [PubMed]

G. P. Luke, D. Yeager, and S. Y. Emelianov, “Biomedical applications of photoacoustic imaging with exogenous contrast agents,” Ann. Biomed. Eng. 40(2), 422–437 (2012).
[Crossref] [PubMed]

C. L. Bayer, G. P. Luke, and S. Y. Emelianov, “Photoacoustic imaging for medical diagnostics,” Acoust. Today 8(4), 15–23 (2012).
[Crossref] [PubMed]

Lythgoe, M.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Lythgoe, M. F.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Macgowan, C. K.

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

Mallidi, S.

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

Mamou, J.

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

Mancini, M.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Maslov, K.

E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref] [PubMed]

McCormick, S.

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

Miranda, R. C.

S. Bake, J. D. Tingling, and R. C. Miranda, “Ethanol exposure during pregnancy persistently attenuates cranially directed blood flow in the developing fetus: evidence from ultrasound imaging in a murine second trimester equivalent model,” Alcohol. Clin. Exp. Res. 36(5), 748–758 (2012).
[Crossref] [PubMed]

Mission, J. F.

J. O. Lo, J. F. Mission, and A. B. Caughey, “Hypertensive disease of pregnancy and maternal mortality,” Curr. Opin. Obstet. Gynecol. 25(2), 124–132 (2013).
[Crossref] [PubMed]

Mohun, T. J.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Mongan, P. D.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Moss, J.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Mu, J.

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

Nguyen, T. M.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Norris, F.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Norris, F. C.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

O’Donnell, M.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Pallares, P.

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

Pappatà, S.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Pelivanov, I. M.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Perez-Solana, M. L.

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

Phoon, C. K. L.

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Qu, D.

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

Ragucci, M.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Rao, J.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Richardson, L.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Rodriguez, D. P.

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Rosa, A.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Salvatore, M.

A. Greco, M. Ragucci, A. R. D. Coda, A. Rosa, S. Gargiulo, R. Liuzzi, M. Gramanzini, S. Albanese, S. Pappatà, M. Mancini, A. Brunetti, and M. Salvatore, “High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice,” PLoS One 8(10), e77205 (2013).
[Crossref] [PubMed]

Scambler, P.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Scambler, P. J.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Schoenfeld, D.

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

Seed, M.

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

Serianni, R.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Severinghaus, J. W.

J. W. Severinghaus, “Simple, accurate equations for human blood O2 dissociation computations,” J. Appl. Physiol. 46(3), 599–602 (1979).
[PubMed]

J. W. Severinghaus, “Oxyhemoglobin dissociation curve correction for temperature and pH variation in human blood,” J. Appl. Physiol. 12(3), 485–486 (1958).
[PubMed]

Sharma, P.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Sled, J. G.

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

Slevin, J. C.

J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
[Crossref] [PubMed]

Speck, N. A.

A. D. Yzaguirre and N. A. Speck, “Extravascular endothelial and hematopoietic islands form through multiple pathways in midgestation mouse embryos,” Dev. Biol. 415(1), 111–121 (2016).
[Crossref] [PubMed]

Stein, E. W.

E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref] [PubMed]

Stevenson, P.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Swartley, O. M.

O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
[Crossref] [PubMed]

Taylor, G. A.

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Timerman, D.

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

Tingling, J. D.

S. Bake, J. D. Tingling, and R. C. Miranda, “Ethanol exposure during pregnancy persistently attenuates cranially directed blood flow in the developing fetus: evidence from ultrasound imaging in a murine second trimester equivalent model,” Alcohol. Clin. Exp. Res. 36(5), 748–758 (2012).
[Crossref] [PubMed]

Torres-Rovira, L.

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

Treeby, B.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Turnbull, D. H.

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Venkataraman, S.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Via, D.

R. Serianni, J. Barash, T. Bentley, P. Sharma, J. L. Fontana, D. Via, J. Duhm, R. Bunger, and P. D. Mongan, “Porcine-specific hemoglobin saturation measurements,” J. Appl. Physiol. 94, 561–566 (2003).

Wang, L. V.

E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref] [PubMed]

Watanabe, K.

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

Weaver, T.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Weber, J.

J. Weber, P. C. Beard, and S. E. Bohndiek, “Contrast agents for molecular photoacoustic imaging,” Nat. Methods 13(8), 639–650 (2016).
[Crossref] [PubMed]

Wei, C. W.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Weninger, W. J.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Wong, E. Y.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Wong, M. D.

F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Worrad, D. M.

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Xia, J.

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
[Crossref] [PubMed]

Yang, Y.

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
[Crossref] [PubMed]

Yeager, D.

G. P. Luke, D. Yeager, and S. Y. Emelianov, “Biomedical applications of photoacoustic imaging with exogenous contrast agents,” Ann. Biomed. Eng. 40(2), 422–437 (2012).
[Crossref] [PubMed]

Yin, M.

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

Yu, Q.

L. Leatherbury, Q. Yu, and C. W. Lo, “Noninvasive phenotypic analysis of cardiovascular structure and function in fetal mice using ultrasound,” Birth Defects Res. C Embryo Today 69(1), 83–91 (2003).
[Crossref] [PubMed]

Yzaguirre, A. D.

A. D. Yzaguirre and N. A. Speck, “Extravascular endothelial and hematopoietic islands form through multiple pathways in midgestation mouse embryos,” Dev. Biol. 415(1), 111–121 (2016).
[Crossref] [PubMed]

Zhang, E.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
[Crossref] [PubMed]

Zhou, B.

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Zhou, Y. Q.

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

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S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
[PubMed]

Acoust. Today (1)

C. L. Bayer, G. P. Luke, and S. Y. Emelianov, “Photoacoustic imaging for medical diagnostics,” Acoust. Today 8(4), 15–23 (2012).
[Crossref] [PubMed]

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[Crossref] [PubMed]

Ann. Biomed. Eng. (1)

G. P. Luke, D. Yeager, and S. Y. Emelianov, “Biomedical applications of photoacoustic imaging with exogenous contrast agents,” Ann. Biomed. Eng. 40(2), 422–437 (2012).
[Crossref] [PubMed]

Biol. Reprod. (1)

P. Pallares, M. L. Perez-Solana, L. Torres-Rovira, and A. Gonzalez-Bulnes, “Phenotypic characterization by high-resolution three-dimensional magnetic resonance imaging evidences differential effects of embryo genotype on intrauterine growth retardation in NOS3-deficient mice,” Biol. Reprod. 84(5), 866–871 (2011).
[Crossref] [PubMed]

Birth Defects Res. C Embryo Today (1)

L. Leatherbury, Q. Yu, and C. W. Lo, “Noninvasive phenotypic analysis of cardiovascular structure and function in fetal mice using ultrasound,” Birth Defects Res. C Embryo Today 69(1), 83–91 (2003).
[Crossref] [PubMed]

Cancer Res. (1)

A. Bar-Zion, M. Yin, D. Adam, and F. S. Foster, “Functional Flow Patterns and Static Blood Pooling in Tumors Revealed by Combined Contrast-Enhanced Ultrasound and Photoacoustic Imaging,” Cancer Res. 76(15), 4320–4331 (2016).
[Crossref] [PubMed]

Circ. Res. (1)

C. K. L. Phoon, R. P. Ji, O. Aristizábal, D. M. Worrad, B. Zhou, H. S. Baldwin, and D. H. Turnbull, “Embryonic heart failure in NFATc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy,” Circ. Res. 95(1), 92–99 (2004).
[Crossref] [PubMed]

Comp. Med. (1)

S. D. Brown, D. Zurakowski, D. P. Rodriguez, P. S. Dunning, R. J. Hurley, and G. A. Taylor, “Ultrasound diagnosis of mouse pregnancy and gestational staging,” Comp. Med. 56(4), 262–271 (2006).
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J. O. Lo, J. F. Mission, and A. B. Caughey, “Hypertensive disease of pregnancy and maternal mortality,” Curr. Opin. Obstet. Gynecol. 25(2), 124–132 (2013).
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Dev. Biol. (1)

A. D. Yzaguirre and N. A. Speck, “Extravascular endothelial and hematopoietic islands form through multiple pathways in midgestation mouse embryos,” Dev. Biol. 415(1), 111–121 (2016).
[Crossref] [PubMed]

IEEE Trans. Ultrason. Ferroelectr. Freq. Control (1)

C. W. Wei, T. M. Nguyen, J. Xia, B. Arnal, E. Y. Wong, I. M. Pelivanov, and M. O’Donnell, “Real-time integrated photoacoustic and ultrasound (PAUS) imaging system to guide interventional procedures: ex vivo study,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 62(2), 319–328 (2015).
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J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt. 17(6), 061220 (2012).
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E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref] [PubMed]

J. Cereb. Blood Flow Metab. (1)

L. S. Cahill, Y. Q. Zhou, M. Seed, C. K. Macgowan, and J. G. Sled, “Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia,” J. Cereb. Blood Flow Metab. 34(6), 1082–1088 (2014).
[Crossref] [PubMed]

Nat. Methods (1)

J. Weber, P. C. Beard, and S. E. Bohndiek, “Contrast agents for molecular photoacoustic imaging,” Nat. Methods 13(8), 639–650 (2016).
[Crossref] [PubMed]

Nucleic Acids Res. (1)

L. Richardson, S. Venkataraman, P. Stevenson, Y. Yang, J. Moss, L. Graham, N. Burton, B. Hill, J. Rao, R. A. Baldock, and C. Armit, “EMAGE mouse embryo spatial gene expression database: 2014 update,” Nucleic Acids Res. 42(D1), D835–D844 (2014).
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J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
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Radiology (1)

G. P. Luke and S. Y. Emelianov, “Label-free Detection of Lymph Node Metastases with US-guided Functional Photoacoustic Imaging,” Radiology 277(2), 435–442 (2015).
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J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reprod. Biol. Endocrinol. 6(1), 34 (2008).
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Theranostics (1)

S. Mallidi, K. Watanabe, D. Timerman, D. Schoenfeld, and T. Hasan, “Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging,” Theranostics 5(3), 289–301 (2015).
[Crossref] [PubMed]

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O. M. Swartley, J. F. Foley, D. P. Livingston, J. M. Cullen, and S. A. Elmore, “Histology Atlas of the Developing Mouse Hepatobiliary Hemolymphatic Vascular System with Emphasis on Embryonic Days 11.5-18.5 and Early Postnatal Development,” Toxicol. Pathol. 44(5), 705–725 (2016).
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F. C. Norris, M. D. Wong, N. D. E. Greene, P. J. Scambler, T. Weaver, W. J. Weninger, T. J. Mohun, R. M. Henkelman, and M. F. Lythgoe, “A coming of age: advanced imaging technologies for characterising the developing mouse,” Trends Genet. 29(12), 700–711 (2013).
[Crossref] [PubMed]

Ultrasound Med. Biol. (1)

O. Aristizábal, J. Mamou, J. A. Ketterling, and D. H. Turnbull, “High-throughput, high-frequency 3-D ultrasound for in utero analysis of embryonic mouse brain development,” Ultrasound Med. Biol. 39(12), 2321–2332 (2013).
[Crossref] [PubMed]

Other (3)

P. V. Chitnis, O. Aristizabal, E. Filoux, A. Sampathkumar, J. Mamou, D. H. Turnbull, and J. A. Ketterling, “Combined optoacoustic and high-frequency ultrasound imaging of live mouse embryos,” in Photons Plus Ultrasound: Imaging and Sensing (2012), pp. 822314–822316.

S. Prahl, “Optical Absorption of Hemoglobin.” http://omlc.org/spectra/hemoglobin/

C. Lutzweiler and D. Razansky, “Optoacoustic imaging and tomography: reconstruction approaches and outstanding challenges in image performance and quantification,” in Sensors (Basel) (2013), pp. 7345–7384.

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Figures (4)

Fig. 1
Fig. 1

Linear least squares fitting of 2D images of photoacoustic signal intensity variation with laser wavelength to the optical absorption of oxy- and deoxyhemoglobin, to generate 2D images of sO2. (a) photoacoustic images acquired at multiple laser wavelengths; (b) photoacoustic signal at each pixel is fit to the optical absorption coefficient of oxy- and deoxyhemoglobin to generate a 2D map of sO2 (c).

Fig. 2
Fig. 2

Longitudinal ultrasound-guided photoacoustic images of development. The ultrasound (a-e) provides high resolution images of the anatomy. The photoacoustic signal, overlain on the ultrasound images (f-j) shows signal in tissue which is highly absorbing due to the presence of hemoglobin. All images were acquired with a 40 MHz transducer, and the photoacoustic signal was acquired at 810 nm. Scale bars = 2mm. Uterus (u), embryo (em), fetus (f) and placenta (p) are labeled in the ultrasound images. Photoacoustic skin artifacts have been manually segmented and removed from images.

Fig. 3
Fig. 3

Endogenous photoacoustic contrast in E10.5 and E14.5 concepti. (a) ultrasound-guided photoacoustic image, (b) excised gravid uterine horn segment, (c) Reichart’s membrane (d) yolk sac; and (e) embryo of E10.5 conceptus. (f) ultrasound-guided photoacoustic image, (g) excised gravid uterine horn segment, (h) yolk sac and (i) fetus of E14.5 conceptus. Scale bars = 2mm. placenta (p) and fetus (f) are labeled in the images.

Fig. 4
Fig. 4

Longitudinal in vivo imaging of regional tissue sO2 during development. a) A tissue phantom of porcine blood at varying partial pressure of oxygen was used to generate spectral photoacoustic images, which were fit using the spectral fitting algorithms (measured data). The spectral fitting algorithm results were calibrated using tabulated sO2 vs partial pressure of oxygen (standard). b) The oxygen saturation values resulting from the calibrated fitting algorithms are overlain on the ultrasound anatomy. Intensity of sO2 signal in each image is proportional to the photoacoustic signal intensity. Scale bars = 2mm.

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