Abstract

We report on simultaneous frequency domain optical-resolution photoacoustic and fluorescence microscopy with sub-µm lateral resolution. With the help of a blood smear, we show that photoacoustic and fluorescence images provide complementary information. Furthermore, we compare theoretically predicted signal-to-noise ratios of sinusoidal modulation in frequency domain with pulsed excitation in time domain.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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2015 (1)

2014 (3)

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

P. Mohajerani, S. Kellnberger, and V. Ntziachristos, “Frequency domain optoacoustic tomography using amplitude and phase,” Photoacoustics 2(3), 111–118 (2014).
[Crossref] [PubMed]

2013 (4)

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

A. Hochreiner, J. Bauer-Marschallinger, P. Burgholzer, B. Jakoby, and T. Berer, “Non-contact photoacoustic imaging using a fiber based interferometer with optical amplification,” Biomed. Opt. Express 4(11), 2322–2331 (2013).
[Crossref] [PubMed]

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

2012 (4)

2011 (3)

2010 (5)

R. L. Shelton and B. E. Applegate, “Ultrahigh resolution photoacoustic microscopy via transient absorption,” Biomed. Opt. Express 1(2), 676–686 (2010).
[Crossref] [PubMed]

C. Zhang, K. Maslov, and L. V. Wang, “Subwavelength-resolution label-free photoacoustic microscopy of optical absorption in vivo,” Opt. Lett. 35(19), 3195–3197 (2010).
[Crossref] [PubMed]

A. Petschke and P. J. La Rivière, “Comparison of intensity-modulated continuous-wave lasers with a chirped modulation frequency to pulsed lasers for photoacoustic imaging applications,” Biomed. Opt. Express 1(4), 1188–1195 (2010).
[Crossref] [PubMed]

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

2009 (4)

S. W. Hell and E. Rittweger, “Microscopy: Light from the dark,” Nature 461(7267), 1069–1070 (2009).
[Crossref] [PubMed]

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

Z. Xie, S. Jiao, H. F. Zhang, and C. A. Puliafito, “Laser-scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 34(12), 1771–1773 (2009).
[Crossref] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

2008 (1)

K. Maslov and L. V. Wang, “Photoacoustic imaging of biological tissue with intensity-modulated continuous-wave laser,” J. Biomed. Opt. 13(2), 024006 (2008).
[Crossref] [PubMed]

2007 (1)

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

2006 (2)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

2005 (1)

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[Crossref] [PubMed]

2004 (2)

M. J. Booth and T. Wilson, “Low-cost, frequency-domain, fluorescence lifetime confocal microscopy,” J. Microsc. 214(1), 36–42 (2004).
[Crossref] [PubMed]

H. Urey, “Spot size, depth-of-focus, and diffraction ring intensity formulas for truncated Gaussian beams,” Appl. Opt. 43(3), 620–625 (2004).
[Crossref] [PubMed]

2001 (3)

J. J. Irwin and J. T. Kirchner, “Anemia in Children,” Am. Fam. Physician 64(8), 1379–1386 (2001).
[PubMed]

I. G. Calasso, W. Craig, and G. J. Diebold, “Photoacoustic point source,” Phys. Rev. Lett. 86(16), 3550–3553 (2001).
[Crossref] [PubMed]

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

1999 (1)

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

1985 (1)

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

1984 (1)

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

1980 (2)

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

A. Rosencwaig and G. Busse, “High-resolution photoacoustic thermal-wave microscopy,” Appl. Phys. Lett. 36(9), 725 (1980).
[Crossref]

1880 (1)

A. G. Bell, “Upon the production of sound by radiant energy,” Am. J. Sci. 20, 305–324 (1880).
[Crossref]

Alexander, J. D.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Alwi, R.

Applegate, B. E.

Armstrong, J. B.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Asghari-Khiavi, M.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Bambery, K. R.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Bauer-Marschallinger, J.

Bell, A. G.

A. G. Bell, “Upon the production of sound by radiant energy,” Am. J. Sci. 20, 305–324 (1880).
[Crossref]

Berer, T.

Berndl, E. S. L.

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

Biris, A. S.

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

Blair-West, J. R.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Booth, M. J.

M. J. Booth and T. Wilson, “Low-cost, frequency-domain, fluorescence lifetime confocal microscopy,” J. Microsc. 214(1), 36–42 (2004).
[Crossref] [PubMed]

Brett, M.

Buckingham, D. W.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Burgholzer, P.

Busse, G.

A. Rosencwaig and G. Busse, “High-resolution photoacoustic thermal-wave microscopy,” Appl. Phys. Lett. 36(9), 725 (1980).
[Crossref]

Calasso, I. G.

I. G. Calasso, W. Craig, and G. J. Diebold, “Photoacoustic point source,” Phys. Rev. Lett. 86(16), 3550–3553 (2001).
[Crossref] [PubMed]

Carter, G. M.

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

Chapman, H. L.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Chen, Y.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

Conchello, J.-A.

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[Crossref] [PubMed]

Cooke, B. M.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Cornelius, L. A.

C. P. Favazza, O. Jassim, L. A. Cornelius, and L. V. Wang, “In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus,” J. Biomed. Opt. 16(1), 016015 (2011).
[Crossref] [PubMed]

Craig, W.

I. G. Calasso, W. Craig, and G. J. Diebold, “Photoacoustic point source,” Phys. Rev. Lett. 86(16), 3550–3553 (2001).
[Crossref] [PubMed]

Cripe, W. S.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Danielli, A.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

Deliolanis, N. C.

Dervishi, E.

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

Diebold, G. J.

I. G. Calasso, W. Craig, and G. J. Diebold, “Photoacoustic point source,” Phys. Rev. Lett. 86(16), 3550–3553 (2001).
[Crossref] [PubMed]

Dorn, G. W.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

Eisinger, J.

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

et,

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Favazza, C. P.

C. P. Favazza, O. Jassim, L. A. Cornelius, and L. V. Wang, “In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus,” J. Biomed. Opt. 16(1), 016015 (2011).
[Crossref] [PubMed]

Favro, L. D.

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

Flores, J.

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

Forcht, M.

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

Galanzha, E. I.

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

Gao, L.

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

Garcia-Uribe, A.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

Hajireza, P.

Harke, B.

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

Harms, P.

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

Hell, S. W.

S. W. Hell and E. Rittweger, “Microscopy: Light from the dark,” Nature 461(7267), 1069–1070 (2009).
[Crossref] [PubMed]

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

Herman, P.

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

Hochreiner, A.

Hu, S.

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[Crossref] [PubMed]

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

Irwin, J. J.

J. J. Irwin and J. T. Kirchner, “Anemia in Children,” Am. Fam. Physician 64(8), 1379–1386 (2001).
[PubMed]

Jakoby, B.

Jassim, O.

C. P. Favazza, O. Jassim, L. A. Cornelius, and L. V. Wang, “In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus,” J. Biomed. Opt. 16(1), 016015 (2011).
[Crossref] [PubMed]

Jiao, S.

Kellnberger, S.

P. Mohajerani, S. Kellnberger, and V. Ntziachristos, “Frequency domain optoacoustic tomography using amplitude and phase,” Photoacoustics 2(3), 111–118 (2014).
[Crossref] [PubMed]

S. Kellnberger, N. C. Deliolanis, D. Queirós, G. Sergiadis, and V. Ntziachristos, “In vivo frequency domain optoacoustic tomography,” Opt. Lett. 37(16), 3423–3425 (2012).
[Crossref] [PubMed]

Kim, C.

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

Kirchner, J. T.

J. J. Irwin and J. T. Kirchner, “Anemia in Children,” Am. Fam. Physician 64(8), 1379–1386 (2001).
[PubMed]

Kolios, M. C.

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

Kuo, P. K.

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

La Rivière, P. J.

Lakowicz, J. R.

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

Lashkari, B.

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

Li, C.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

Lichtman, J. W.

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[Crossref] [PubMed]

Lin, H.-J.

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

Ma, R.

Maliwal, B. P.

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

Mandelis, A.

S. Telenkov, R. Alwi, A. Mandelis, and A. Worthington, “Frequency-domain photoacoustic phased array probe for biomedical imaging applications,” Opt. Lett. 36(23), 4560–4562 (2011).
[Crossref] [PubMed]

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

Maslov, K.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

C. Zhang, K. Maslov, J. Yao, and L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[Crossref] [PubMed]

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[Crossref] [PubMed]

C. Zhang, K. Maslov, and L. V. Wang, “Subwavelength-resolution label-free photoacoustic microscopy of optical absorption in vivo,” Opt. Lett. 35(19), 3195–3197 (2010).
[Crossref] [PubMed]

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

K. Maslov and L. V. Wang, “Photoacoustic imaging of biological tissue with intensity-modulated continuous-wave laser,” J. Biomed. Opt. 13(2), 024006 (2008).
[Crossref] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

McNaughton, D.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Mechler, A.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Medda, R.

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

Miranda, R.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Mohajerani, P.

P. Mohajerani, S. Kellnberger, and V. Ntziachristos, “Frequency domain optoacoustic tomography using amplitude and phase,” Photoacoustics 2(3), 111–118 (2014).
[Crossref] [PubMed]

Morris, J. G.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Nedosekin, D. A.

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

Ntziachristos, V.

Petschke, A.

Pouch, J. J.

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

Puliafito, C. A.

Queirós, D.

Ram, N.

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

Rao, G.

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

Razansky, D.

Rittweger, E.

S. W. Hell and E. Rittweger, “Microscopy: Light from the dark,” Nature 461(7267), 1069–1070 (2009).
[Crossref] [PubMed]

Rosencwaig, A.

A. Rosencwaig and G. Busse, “High-resolution photoacoustic thermal-wave microscopy,” Appl. Phys. Lett. 36(9), 725 (1980).
[Crossref]

Sanchez, A.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Sanchez, B.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Sergiadis, G.

Shelton, R. L.

Shoham, S.

Shohet, S. B.

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

Sipior, J.

P. Harms, J. Sipior, N. Ram, G. M. Carter, and G. Rao, “Low cost phase-modulation measurements of nanosecond fluorescence lifetimes using a lock-in amplifier,” Rev. Sci. Instrum. 70(2), 1535 (1999).
[Crossref]

Söntges, S.

Sorge, J.

Stoica, G.

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

Strohm, E. M.

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

E. M. Strohm, E. S. L. Berndl, and M. C. Kolios, “High frequency label-free photoacoustic microscopy of single cells,” Photoacoustics 1(3-4), 49–53 (2013).
[Crossref] [PubMed]

Telenkov, S.

S. Telenkov, R. Alwi, A. Mandelis, and A. Worthington, “Frequency-domain photoacoustic phased array probe for biomedical imaging applications,” Opt. Lett. 36(23), 4560–4562 (2011).
[Crossref] [PubMed]

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

Thomas, R. L.

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

Tyson, J. A.

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

Urey, H.

Walker, D. F.

J. G. Morris, W. S. Cripe, H. L. Chapman, D. F. Walker, J. B. Armstrong, J. D. Alexander, R. Miranda, A. Sanchez, B. Sanchez, J. R. Blair-West, and et, “Selenium deficiency in cattle associated with Heinz bodies and anemia,” Science 223(4635), 491–493 (1984).
[Crossref] [PubMed]

Wang, L.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

Wang, L. V.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

C. Zhang, K. Maslov, J. Yao, and L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[Crossref] [PubMed]

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[Crossref] [PubMed]

C. P. Favazza, O. Jassim, L. A. Cornelius, and L. V. Wang, “In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus,” J. Biomed. Opt. 16(1), 016015 (2011).
[Crossref] [PubMed]

C. Zhang, K. Maslov, and L. V. Wang, “Subwavelength-resolution label-free photoacoustic microscopy of optical absorption in vivo,” Opt. Lett. 35(19), 3195–3197 (2010).
[Crossref] [PubMed]

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

K. Maslov and L. V. Wang, “Photoacoustic imaging of biological tissue with intensity-modulated continuous-wave laser,” J. Biomed. Opt. 13(2), 024006 (2008).
[Crossref] [PubMed]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

Wang, Y.

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

Willig, K. I.

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

Wilson, T.

M. J. Booth and T. Wilson, “Low-cost, frequency-domain, fluorescence lifetime confocal microscopy,” J. Microsc. 214(1), 36–42 (2004).
[Crossref] [PubMed]

Winkler, A. M.

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

Wood, B. R.

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Worthington, A.

Xie, Z.

Xing, D.

Xu, M.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

Yang, S.

Yao, J.

C. Zhang, K. Maslov, J. Yao, and L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[Crossref] [PubMed]

Ye, F.

Zemp, R.

Zhang, C.

C. Zhang, K. Maslov, J. Yao, and L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[Crossref] [PubMed]

C. Zhang, K. Maslov, and L. V. Wang, “Subwavelength-resolution label-free photoacoustic microscopy of optical absorption in vivo,” Opt. Lett. 35(19), 3195–3197 (2010).
[Crossref] [PubMed]

Zhang, H. F.

Z. Xie, S. Jiao, H. F. Zhang, and C. A. Puliafito, “Laser-scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 34(12), 1771–1773 (2009).
[Crossref] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

Zharov, V. P.

D. A. Nedosekin, E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, “Super-Resolution Nonlinear Photothermal Microscopy,” Small 10(1), 135–142 (2014).
[Crossref] [PubMed]

Am. Fam. Physician (1)

J. J. Irwin and J. T. Kirchner, “Anemia in Children,” Am. Fam. Physician 64(8), 1379–1386 (2001).
[PubMed]

Am. J. Sci. (1)

A. G. Bell, “Upon the production of sound by radiant energy,” Am. J. Sci. 20, 305–324 (1880).
[Crossref]

Analyst (Lond.) (1)

M. Asghari-Khiavi, B. R. Wood, A. Mechler, K. R. Bambery, D. W. Buckingham, B. M. Cooke, and D. McNaughton, “Correlation of atomic force microscopy and Raman micro-spectroscopy to study the effects of ex vivo treatment procedures on human red blood cells,” Analyst (Lond.) 135(3), 525–530 (2010).
[Crossref] [PubMed]

Appl. Opt. (1)

Appl. Phys. Lett. (2)

L. D. Favro, P. K. Kuo, J. J. Pouch, and R. L. Thomas, “Photoacoustic microscopy of an integrated circuit,” Appl. Phys. Lett. 36(12), 953 (1980).
[Crossref]

A. Rosencwaig and G. Busse, “High-resolution photoacoustic thermal-wave microscopy,” Appl. Phys. Lett. 36(9), 725 (1980).
[Crossref]

Biomed. Opt. Express (4)

Blood (1)

J. Eisinger, J. Flores, J. A. Tyson, and S. B. Shohet, “Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: evidence for intracellular heme catabolism,” Blood 65(4), 886–893 (1985).
[PubMed]

IEEE Trans. Biomed. Eng. (1)

Y. Wang, K. Maslov, C. Kim, S. Hu, and L. V. Wang, “Integrated Photoacoustic and Fluorescence Confocal Microscopy,” IEEE Trans. Biomed. Eng. 57(10), 2576–2578 (2010).
[Crossref] [PubMed]

J. Appl. Phys. (1)

S. Telenkov, A. Mandelis, B. Lashkari, and M. Forcht, “Frequency-domain photothermoacoustics: Alternative imaging modality of biological tissues,” J. Appl. Phys. 105(10), 102029 (2009).
[Crossref]

J. Biomed. Opt. (4)

A. Danielli, K. Maslov, A. Garcia-Uribe, A. M. Winkler, C. Li, L. Wang, Y. Chen, G. W. Dorn, and L. V. Wang, “Label-free photoacoustic nanoscopy,” J. Biomed. Opt. 19(8), 086006 (2014).
[Crossref] [PubMed]

C. Zhang, K. Maslov, J. Yao, and L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[Crossref] [PubMed]

K. Maslov and L. V. Wang, “Photoacoustic imaging of biological tissue with intensity-modulated continuous-wave laser,” J. Biomed. Opt. 13(2), 024006 (2008).
[Crossref] [PubMed]

C. P. Favazza, O. Jassim, L. A. Cornelius, and L. V. Wang, “In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus,” J. Biomed. Opt. 16(1), 016015 (2011).
[Crossref] [PubMed]

J. Biophotonics (1)

L. Gao, L. Wang, C. Li, A. Garcia-Uribe, and L. V. Wang, “Photothermal bleaching in time-lapse photoacoustic microscopy,” J. Biophotonics 6(6-7), 543–548 (2013).
[Crossref] [PubMed]

J. Microsc. (2)

M. J. Booth and T. Wilson, “Low-cost, frequency-domain, fluorescence lifetime confocal microscopy,” J. Microsc. 214(1), 36–42 (2004).
[Crossref] [PubMed]

P. Herman, B. P. Maliwal, H.-J. Lin, and J. R. Lakowicz, “Frequency-domain fluorescence microscopy with the LED as a light source,” J. Microsc. 203(2), 176–181 (2001).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

Nat. Methods (2)

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[Crossref] [PubMed]

K. I. Willig, B. Harke, R. Medda, and S. W. Hell, “STED microscopy with continuous wave beams,” Nat. Methods 4(11), 915–918 (2007).
[Crossref] [PubMed]

Nat. Photonics (1)

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

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[Crossref] [PubMed]

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Figures (3)

Fig. 1
Fig. 1

Schematic of the setup. A function generator (f-gen) is used to modulate a cw diode laser (laser 405 nm). Laser light is focused onto the sample by an objective lens (20 × , NA = 0.5). Photoacoustic and luminescence signals are measured via a hydrophone and an avalanche photo-diode (APD), respectively. The lock-in amplifiers (LIA) are set to the modulation frequency. The 3D scanning stage is symbolized by the xyz coordinate system.

Fig. 2
Fig. 2

(a) fOR-PAM image of a chromium line target with 120 lines/mm. (b) Profile of the photoacoustic image along the red line.

Fig. 3
Fig. 3

fOR-PAM image (a) and simultaneously obtained luminescence image (b) of human red blood cells. (c) Overlay of the photoacoustic and the luminescence image. (d) Bright-field image of the same region.

Tables (1)

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Table 1 SNR ratios for 4ns pulsed excitation and sinusoidal modulation

Equations (15)

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s Kλ 2NA ,
K=1.654 0.105a w + 0.28 a 2 w 2 .
p(t)= σ β 1 4π c p r E θ 2 d d τ ^ f( τ ^ ).
I G (t)= E G τ G π exp( t 2 τ G 2 ),
p G (t) 2t E G τ G 3 π exp( t 2 τ G 2 ).
p G,max 2 eπ E G τ G 2 .
I S ( t )= E S 2π τ S ( 1+sin( t/ τ S ) ),
p S (t)2π f S 2 E S cos( 2π f S t )=2π I 0 f S cos( 2π f S t ).
p S,max 2π I 0 f S
p G,max p S,max = 1 2πe 1 π E G I 0 1 τ G 2 f S 1 4π E G I 0 1 τ G 2 f S .
χ= B Det B LIA ,
B LIA = 1 2π τ LIA .
SNR G SNR S = p G,max ξ NEP NEP p S,max χ 1 4π E G I 0 1 τ G 2 f S ξ χ .
I 0,max =1.1 10 4 × (τ/sec) 0.75 W/m 2 .
PA S (t) I 0 e k( I 0 )t

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