Abstract

Photoacoustic microscopy (PAM) is an attractive imaging tool that complements established optical microscopic modalities by providing additional molecular specificities through imaging optical absorption contrast. While the development of optical resolution photoacoustic microscopy (ORPAM) offers high lateral resolution, the acoustically determined axial resolution is limited due to the constraint in ultrasonic detection bandwidth. ORPAM with isometric spatial resolution along both axial and lateral directions is yet to be developed. Although recently developed sophisticated optical illumination and reconstruction methods offer improved axial resolution in ORPAM, the image acquisition procedures are rather complicated, limiting their capabilities for high-speed imaging and being easily integrated with established optical microscopic modalities. Here we report an isometric ORPAM based on an optically transparent micro-ring resonator ultrasonic detector and a commercial inverted microscope platform. Owing to the superior spatial resolution and the ease of integrating our ORPAM with established microscopic modalities, single-cell imaging with extrinsic fluorescence staining, intrinsic autofluorescence, and optical absorption can be achieved simultaneously. This technique holds promise to greatly improve the accessibility of PAM to broader biomedical researchers.

© 2015 Optical Society of America

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References

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    [Crossref]
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    [Crossref]
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  45. A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, F. G. Holz, “Two-photon-excited fluorescence imaging of human RPE cells with a femtosecond Ti:sapphire laser,” Investig. Ophthalmol. Vis. Sci. 47, 4553–4557 (2006).
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2014 (6)

B. Rao, F. Soto, D. Kerschensteiner, L. V. Wang, “Integrated photoacoustic, confocal, and two-photon microscope,” J. Biomed. Opt. 19, 36002 (2014).
[Crossref]

H. Li, B. Dong, Z. Zhang, C. Sun, H. F. Zhang, “A transparent broadband ultrasonic detector based on micro-ring resonator for functional photoacoustic imaging,” Sci. Rep. 4, 4496 (2014).

Z. Zhang, B. Dong, H. Li, F. Zhou, H. F. Zhang, C. Sun, “Theoretical and experimental studies of distance dependent response of micro-ring resonator-based ultrasonic detectors for photoacoustic microscopy,” J. Appl. Phys. 116, 144501 (2014).
[Crossref]

M. Zareba, C. M. B. Skumatz, T. J. Sarna, J. M. Burke, “Photic injury to cultured RPE varies among individual cells in proportion to their endogenous lipofuscin content as modulated by their melanosome content,” Investig. Ophthalmol. Vis. Sci. 55, 4982–4990 (2014).
[Crossref]

J. Yao, L. Wang, C. Li, C. Zhang, L. V. Wang, “Photoimprint photoacoustic microscopy for three-dimensional label-free subdiffraction imaging,” Phys. Rev. Lett. 112, 014302 (2014).
[Crossref]

L. Zhu, L. Li, L. Gao, L. V. Wang, “Multiview optical resolution photoacoustic microscopy,” Optica 1, 217–222 (2014).
[Crossref]

2013 (4)

Y. Zhou, J. Liang, K. I. Maslov, L. V. Wang, “Calibration-free in vivo transverse blood flowmetry based on cross correlation of slow time profiles from photoacoustic microscopy,” Opt. Lett. 38, 3882–3885 (2013).
[Crossref]

W. Song, W. Liu, H. F. Zhang, “Laser-scanning Doppler photoacoustic microscopy based on temporal correlation,” Appl. Phys. Lett. 102, 203501 (2013).
[Crossref]

M. Mehrmohammadi, S. J. Yoon, S. Y. Emelianov, “Photoacoustic imaging for cancer detection and staging,” Curr. Mol. Imaging 2, 89–105 (2013).

J. Yao, J. Xia, K. Maslov, M. Naziriavanaki, V. Tsytsarev, A. V. Demchenko, L. V. Wang, “Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo,” NeuroImaging 64, 257–266 (2013).

2012 (4)

M. R. Chatni, J. Xia, R. Sohn, K. Maslov, Z. Guo, Y. Zhang, K. Wang, Y. Xia, M. Anastasio, J. Arbeit, L. V. Wang, “Tumor glucose metabolism imaged in vivo in small animals with whole-body photoacoustic computed tomography,” J. Biomed. Opt. 17, 0760121 (2012).
[Crossref]

J. Yao, K. I. Maslov, L. V. Wang, “In vivo photoacoustic tomography of total blood flow and potential imaging of cancer angiogenesis and hypermetabolism,” Technol. Cancer Res. Treat. 11, 301–307 (2012).

J. Bauer-Marschallinger, T. Berer, H. Grun, H. Roitner, B. Reitinger, P. Burgholzer, “Broadband high-frequency measurement of ultrasonic attenuation of tissues and liquids,” IEEE Trans. Ultrason. Ferroelectr Freq. Control. 59, 2631–2645 (2012).

L. V. Wang, S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335, 1458–1462 (2012).
[Crossref]

2011 (7)

C. Jing, V. W. Cornish, “Chemical tags for labeling proteins inside living cells,” Acc. Chem. Res. 44, 784–792 (2011).

X. Y. Zhang, H. F. Zhang, C. A. Puliafito, S. L. Jiao, “Simultaneous in vivo imaging of melanin and lipofuscin in the retina with photoacoustic ophthalmoscopy and autofluorescence imaging,” J. Biomed. Opt. 16, 080504 (2011).
[Crossref]

H. F. Zhang, C. A. Puliafito, S. L. Jiao, “Photoacoustic ophthalmoscopy for in vivo retinal imaging: current status and prospects,” Ophthal. Surg. Lasers Imag. 42, S106–S115 (2011).

S. Hu, K. Maslov, L. V. Wang, “Three-dimensional optical-resolution photoacoustic microscopy,” J. Vis. Express 3, 2729 (2011).

P. C. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1, 602–631 (2011).

T. Ling, S.-L. Chen, L. J. Guo, “Fabrication and characterization of high Q polymer micro-ring resonator and its application as a sensitive ultrasonic detector,”Opt. Express 19, 861–869 (2011).
[Crossref]

T. Liu, Q. Wei, J. Wang, S. L. Jiao, H. F. Zhang, “Combined photoacoustic microscopy and optical coherence tomography can measure metabolic rate of oxygen,” Biomed. Opt. Express 2, 1359–1365 (2011).
[Crossref]

2010 (4)

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

X. Zhang, M. Jiang, A. A. Fawzi, X. Li, K. K. Shung, C. A. Puliafito, H. F. Zhang, S. Jiao, “Simultaneous dual molecular contrasts provided by the absorbed photons in photoacoustic microscopy,” Opt. Lett. 35, 4018–4020 (2010).
[Crossref]

Y. Wang, K. Maslov, C. Kim, S. Hu, L. V. Wang, “Integrated photoacoustic and fluorescence confocal microscopy,” IEEE Trans. Biomed. Eng. 57, 2576–2578 (2010).
[Crossref]

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, L. V. Wang, “In vivo molecular photoacoustic tomography of melanomas targeted by bio-conjugated gold nanocages,” ACS Nano 4, 4559–4564 (2010).
[Crossref]

2009 (2)

M. S. Yavuz, Y. Cheng, J. Chen, C. M. Cobley, Q. Zhang, M. Rycenga, J. Xie, C. H. Kim, K. H. Song, A. G. Schwartz, L. V. Wang, Y. Xia, “Gold nanocages covered by smart polymers for controlled release with near-infrared light,” Nat. Mater. 8, 935–939 (2009).
[Crossref]

X. W. Zhuang, “Nano-imaging with STORM,” Nat. Photonics 3, 365–367 (2009).
[Crossref]

2008 (3)

U. Resch-Genger, M. Grabolle, S. Cavaliere-Jaricot, R. Nitschke, T. Nann, “Quantum dots versus organic dyes as fluorescent labels,” Nat. Methods 5, 763–775 (2008).
[Crossref]

Y. Wang, R. K. Wang, “Photoacoustic recovery of an absolute optical absorption coefficient with an exact solution of a wave equation,” Phys Med. Biol. 53, 6167–6177 (2008).

V. L. Bonilha, “Age and disease-related structural changes in the retinal pigment epithelium,” Clin. Ophthalmol. 2, 413–424 (2008).

2007 (3)

H. F. Zhang, K. Maslov, L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protocols 2, 797–804 (2007).

P. Belenky, K. L. Bogan, C. Brenner, “NAD+ metabolism in health and disease,” Trends Biochem. Sci. 32, 12–19 (2007).
[Crossref]

S. W. Hell, “Far-field optical nanoscopy,” Science 316, 1153–1158 (2007).
[Crossref]

2006 (4)

L. Perelman, “Optical diagnostic technology based on light scattering spectroscopy for early cancer detection,” Expert Rev. Med. Dev. 3, 787–803 (2006).

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

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, F. G. Holz, “Two-photon-excited fluorescence imaging of human RPE cells with a femtosecond Ti:sapphire laser,” Investig. Ophthalmol. Vis. Sci. 47, 4553–4557 (2006).
[Crossref]

2005 (1)

B. L. Seagle, E. M. Gasyna, W. F. Mieler, J. R. Norris, “Photoprotection of human retinal pigment epithelium cells against blue light-induced apoptosis by melanin free radicals from Sepia officinalis,” Proc. Natl. Acad. Sci. USA 103, 16644–16648 (2005).

2000 (1)

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, M. S. Feld, T. McGillican, “Detection of preinvasive cancer cells in situ,” Nature 406, 35–36 (2000).
[Crossref]

1999 (1)

S. Weiss, “Fluorescence spectroscopy of single biomolecules,” Science 283, 1676–1683 (1999).
[Crossref]

1998 (1)

L. T. Perelman, V. Backman, M. Wallace, G. Zonios, R. Manoharan, A. Nusrat, S. Shields, M. Seiler, C. Lima, T. Hamano, I. Itzkan, J. Van Dam, J. M. Crawford, M. S. Feld, “Observation of periodic fine structure in reflectance from biological tissue: a new technique for measuring nuclear size distribution,” Phys. Rev. Lett. 80, 627–630 (1998).
[Crossref]

1994 (1)

M. Eigen, R. Rigler, “Sorting single molecules–application to diagnostics and evolutionary biotechnology,” Proc. Natl. Acad. Sci. USA 91, 5740–5747 (1994).

1990 (2)

W. Denk, J. H. Strickler, W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[Crossref]

B. Hadimioglu, B. T. Khuri-Yakub, “Polymer films as acoustic matching layers,” Proc. IEEE 3, 1337–1340 (1990).

Anastasio, M.

M. R. Chatni, J. Xia, R. Sohn, K. Maslov, Z. Guo, Y. Zhang, K. Wang, Y. Xia, M. Anastasio, J. Arbeit, L. V. Wang, “Tumor glucose metabolism imaged in vivo in small animals with whole-body photoacoustic computed tomography,” J. Biomed. Opt. 17, 0760121 (2012).
[Crossref]

Anderson, D.

G. S. Hageman, K. Gehrs, L. V. Johnson, D. Anderson, “Webvision: the organization of the retina and visual system,” in Age-Related Macular Degeneration (AMD), H. Kolb, E. Fernandez, R. Nelson, eds. (University of Utah Health Sciences Center, 2008).

Applegate, B. E.

Arbeit, J.

M. R. Chatni, J. Xia, R. Sohn, K. Maslov, Z. Guo, Y. Zhang, K. Wang, Y. Xia, M. Anastasio, J. Arbeit, L. V. Wang, “Tumor glucose metabolism imaged in vivo in small animals with whole-body photoacoustic computed tomography,” J. Biomed. Opt. 17, 0760121 (2012).
[Crossref]

Arendt, J. T.

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, M. S. Feld, T. McGillican, “Detection of preinvasive cancer cells in situ,” Nature 406, 35–36 (2000).
[Crossref]

Au, L.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, L. V. Wang, “In vivo molecular photoacoustic tomography of melanomas targeted by bio-conjugated gold nanocages,” ACS Nano 4, 4559–4564 (2010).
[Crossref]

Backman, V.

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, M. S. Feld, T. McGillican, “Detection of preinvasive cancer cells in situ,” Nature 406, 35–36 (2000).
[Crossref]

L. T. Perelman, V. Backman, M. Wallace, G. Zonios, R. Manoharan, A. Nusrat, S. Shields, M. Seiler, C. Lima, T. Hamano, I. Itzkan, J. Van Dam, J. M. Crawford, M. S. Feld, “Observation of periodic fine structure in reflectance from biological tissue: a new technique for measuring nuclear size distribution,” Phys. Rev. Lett. 80, 627–630 (1998).
[Crossref]

Badizadegan, K.

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, M. S. Feld, T. McGillican, “Detection of preinvasive cancer cells in situ,” Nature 406, 35–36 (2000).
[Crossref]

Bauer-Marschallinger, J.

J. Bauer-Marschallinger, T. Berer, H. Grun, H. Roitner, B. Reitinger, P. Burgholzer, “Broadband high-frequency measurement of ultrasonic attenuation of tissues and liquids,” IEEE Trans. Ultrason. Ferroelectr Freq. Control. 59, 2631–2645 (2012).

Beard, P. C.

P. C. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1, 602–631 (2011).

Belenky, P.

P. Belenky, K. L. Bogan, C. Brenner, “NAD+ metabolism in health and disease,” Trends Biochem. Sci. 32, 12–19 (2007).
[Crossref]

Berer, T.

J. Bauer-Marschallinger, T. Berer, H. Grun, H. Roitner, B. Reitinger, P. Burgholzer, “Broadband high-frequency measurement of ultrasonic attenuation of tissues and liquids,” IEEE Trans. Ultrason. Ferroelectr Freq. Control. 59, 2631–2645 (2012).

Betzig, E.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Bille, J. F.

A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, F. G. Holz, “Two-photon-excited fluorescence imaging of human RPE cells with a femtosecond Ti:sapphire laser,” Investig. Ophthalmol. Vis. Sci. 47, 4553–4557 (2006).
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Bindewald-Wittich, A.

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Supplementary Material (3)

» Supplement 1: PDF (748 KB)     
» Media 2: MP4 (923 KB)     
» Media 3: MP4 (1061 KB)     

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Figures (3)

Fig. 1.
Fig. 1.

Schematic of the multimodality microscopy system. (a) An integrated microscopic system combining laser-scanning confocal microscopy and PAM was realized by an optically transparent MRR ultrasonic detector. The inset illustrates a magnified view of the placement of the fiber coupled MRR ultrasonic detector and specimen. (b) Illustration of MRR detection of laser-induced PA waves. (c) A representative transmission spectrum exhibits a pronounced resonance dip under the critical coupling condition (black circle) and its corresponding Lorenz fitting (red line). Inset is the numerical simulation of the electric field distribution, which shows the fundamental TM mode in the waveguide. Using a narrow-band laser source (blue line), the pressure-induced resonance shift (dashed red line) can be measured as the amplitude modulation of the transmitted optical signal. (d) Time-resolved PA pulse signal measured by the MRR ultrasonic detector. (e) Its corresponding power spectrum shows an ultra broadband frequency response.

Fig. 2.
Fig. 2.

PAM imaging of single RBCs in a mouse blood smear. (a) Trans-illuminated optical microscopic image. (b) PA maximum amplitude projection image of individual RBCs. Scale bars, 10 μm. (c) Magnified PAM projection image of a single RBC along the x y plane. Scale bar, 2 μm. (d) Cross-sectional image of the same RBC along the x z plane. (e) 3D visualization of the RBC (see Media 1).

Fig. 3.
Fig. 3.

Simultaneous PAM and fluorescence confocal imaging of a human RPE flat mount. (a) Projection PAM image of the RPE along the x y plane. (b) Cross-sectional PAM image along the x z plane. (c) 3D visualization of the RPE cells imaged by PAM (Media 2). (d) Actin stained confocal imaging highlights the boundaries of the RPE cells. (e) Autofluorescence confocal image shows the distribution of lipofuscin. (f) Overlaid image of all the three modalities acquired simultaneously. Scale bars, 10 μm.

Metrics