Abstract

Combining different contrast mechanisms to achieve simultaneous multimodal imaging is always desirable but is challenging due to the various optical and hardware requirements for different imaging systems. We developed a multimodal microscopic optical imaging system with the capability of providing comprehensive structural, functional and molecular information of living tissues. This imaging system integrated photoacoustic microscopy (PAM), optical coherence tomography (OCT), optical Doppler tomography (ODT) and confocal fluorescence microscopy in one platform. By taking advantage of the depth resolving capability of OCT, we developed a novel OCT-guided surface contour scanning methodology for dynamic focusing adjustment. We have conducted phantom, in vivo, and ex vivo tests to demonstrate the capability of the multimodal imaging system for providing comprehensive microscopic information of biological tissues. Integrating all the aforementioned imaging modalities with OCT-guided dynamic focusing for simultaneous multimodal imaging has promising potential for preclinical research and clinical practice in the future.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2016 (5)

W. Liu and H. F. Zhang, “Photoacoustic imaging of the eye: A mini review,” Photoacoustics 4(3), 112–123 (2016).
[Crossref] [PubMed]

W. Song, Q. Xu, Y. Zhang, Y. Zhan, W. Zheng, and L. Song, “Fully integrated reflection-mode photoacoustic, two-photon, and second harmonic generation microscopy in vivo,” Sci. Rep. 6(1), 32240 (2016).
[Crossref] [PubMed]

Z. Nafar, M. Jiang, R. Wen, and S. Jiao, “Visible-light optical coherence tomography-based multimodal retinal imaging for improvement of fluorescent intensity quantification,” Biomed. Opt. Express 7(9), 3220–3229 (2016).
[Crossref] [PubMed]

B. Ning, N. Sun, R. Cao, R. Chen, K. Kirk Shung, J. A. Hossack, J.-M. Lee, Q. Zhou, and S. Hu, “Ultrasound-aided multi-parametric photoacoustic microscopy of the mouse brain,” Sci. Rep. 5(1), 18775 (2016).
[Crossref] [PubMed]

W. H. Jang, S. Shim, T. Wang, Y. Yoon, W.-S. Jang, J. K. Myung, S. Park, and K. H. Kim, “In vivo characterization of early-stage radiation skin injury in a mouse model by two-photon microscopy,” Sci. Rep. 6(1), 19216 (2016).
[Crossref] [PubMed]

2015 (5)

T. Berer, E. Leiss-Holzinger, A. Hochreiner, J. Bauer-Marschallinger, and A. Buchsbaum, “Multimodal noncontact photoacoustic and optical coherence tomography imaging using wavelength-division multiplexing,” J. Biomed. Opt. 20(4), 46013 (2015).
[Crossref] [PubMed]

D. Soliman, G. J. Tserevelakis, M. Omar, and V. Ntziachristos, “Combining microscopy with mesoscopy using optical and optoacoustic label-free modes,” Sci. Rep. 5(1), 12902 (2015).
[Crossref] [PubMed]

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

J. Kim, D. Lee, U. Jung, and C. Kim, “Photoacoustic imaging platforms for multimodal imaging,” Ultrasonography 34(2), 88–97 (2015).
[Crossref] [PubMed]

2014 (6)

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

J. You, C. Du, N. D. Volkow, and Y. Pan, “Optical coherence Doppler tomography for quantitative cerebral blood flow imaging,” Biomed. Opt. Express 5(9), 3217–3230 (2014).
[Crossref] [PubMed]

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

J. Yao and L. V. Wang, “Sensitivity of photoacoustic microscopy,” Photoacoustics 2(2), 87–101 (2014).
[Crossref] [PubMed]

C. Yeh, B. Soetikno, S. Hu, K. I. Maslov, and L. V. Wang, “Microvascular quantification based on contour-scanning photoacoustic microscopy,” J. Biomed. Opt. 19(9), 96011 (2014).
[Crossref] [PubMed]

M. Jiang, T. Liu, X. Liu, and S. Jiao, “Simultaneous optical coherence tomography and lipofuscin autofluorescence imaging of the retina with a single broadband light source at 480nm,” Biomed. Opt. Express 5(12), 4242–4248 (2014).
[Crossref] [PubMed]

2013 (6)

C. Dai, X. Liu, H. F. Zhang, C. A. Puliafito, and S. Jiao, “Absolute retinal blood flow measurement with a dual-beam Doppler optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(13), 7998–8003 (2013).
[Crossref] [PubMed]

C. Dai, X. Liu, H. F. Zhang, C. A. Puliafito, and S. Jiao, “Absolute retinal blood flow measurement with a dual-beam Doppler optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(13), 7998–8003 (2013).
[Crossref] [PubMed]

P. J. Keller, “Imaging morphogenesis: technological advances and biological insights,” Science 340(6137), 1234168 (2013).
[Crossref] [PubMed]

A. P. Cherecheanu, G. Garhofer, D. Schmidl, R. Werkmeister, and L. Schmetterer, “Ocular perfusion pressure and ocular blood flow in glaucoma,” Curr. Opin. Pharmacol. 13(1), 36–42 (2013).
[Crossref] [PubMed]

S. P. Chong, T. Lai, Y. Zhou, and S. Tang, “Tri-modal microscopy with multiphoton and optical coherence microscopy/tomography for multi-scale and multi-contrast imaging,” Biomed. Opt. Express 4(9), 1584–1594 (2013).
[Crossref] [PubMed]

X. Cai, Y. S. Zhang, Y. Xia, and L. V. Wang, “Photoacoustic microscopy in tissue engineering,” Mater Today (Kidlington) 16(3), 67–77 (2013).
[Crossref] [PubMed]

2012 (1)

C. Dai, X. Liu, and S. Jiao, “Simultaneous optical coherence tomography and autofluorescence microscopy with a single light source,” J. Biomed. Opt. 17(8), 080502 (2012).
[Crossref] [PubMed]

2011 (2)

2010 (3)

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

E. J. Johnson, “Age-related macular degeneration and antioxidant vitamins: recent findings,” Curr. Opin. Clin. Nutr. Metab. Care 13(1), 28–33 (2010).
[Crossref] [PubMed]

C. Li, C. Pitsillides, J. M. Runnels, D. Côté, and C. P. Lin, “Multiphoton microscopy of live tissues with ultraviolet autofluorescence,” IEEE J. Sel. Top. Quantum Electron. 16(3), 516–523 (2010).
[Crossref]

2009 (3)

J. Klohs, J. Steinbrink, R. Bourayou, S. Mueller, R. Cordell, K. Licha, M. Schirner, U. Dirnagl, U. Lindauer, and A. Wunder, “Near-infrared fluorescence imaging with fluorescently labeled albumin: a novel method for non-invasive optical imaging of blood-brain barrier impairment after focal cerebral ischemia in mice,” J. Neurosci. Methods 180(1), 126–132 (2009).
[Crossref] [PubMed]

R. Ehrlich, N. S. Kheradiya, D. M. Winston, D. B. Moore, B. Wirostko, and A. Harris, “Age-related ocular vascular changes,” Graefes Arch. Clin. Exp. Ophthalmol. 247(5), 583–591 (2009).
[Crossref] [PubMed]

C. Balas, “Review of biomedical optical imaging—a powerful, non-invasive, non-ionizing technology for improving in vivo diagnosis,” Meas. Sci. Technol. 20(10), 104020 (2009).
[Crossref]

2008 (1)

2007 (1)

2006 (1)

J.-T. Oh, M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 34032 (2006).
[PubMed]

2005 (3)

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

S. Jiao, R. Knighton, X. Huang, G. Gregori, and C. Puliafito, “Simultaneous acquisition of sectional and fundus ophthalmic images with spectral-domain optical coherence tomography,” Opt. Express 13(2), 444–452 (2005).
[Crossref] [PubMed]

J. R. Sparrow and M. Boulton, “RPE lipofuscin and its role in retinal pathobiology,” Exp. Eye Res. 80(5), 595–606 (2005).
[Crossref] [PubMed]

2004 (1)

2003 (2)

Z. Földes-Papp, U. Demel, and G. P. Tilz, “Laser scanning confocal fluorescence microscopy: an overview,” Int. Immunopharmacol. 3(13-14), 1715–1729 (2003).
[Crossref] [PubMed]

C.-J. Chang and K.-H. Hou, “High-resolution optical Doppler tomography for in vitro and in vivo fluid flow dynamics,” Chang Gung Med. J. 26(6), 403–411 (2003).
[PubMed]

2002 (2)

M. Gupta, A. M. Rollins, J. A. Izatt, and I. R. Efimov, “Imaging of the atrioventricular node using optical coherence tomography,” J. Cardiovasc. Electrophysiol. 13(1), 95 (2002).
[Crossref] [PubMed]

V. Ntziachristos, C.-H. Tung, C. Bremer, and R. Weissleder, “Fluorescence molecular tomography resolves protease activity in vivo,” Nat. Med. 8(7), 757–760 (2002).
[Crossref] [PubMed]

2000 (2)

S. Brand, J. M. Poneros, B. E. Bouma, G. J. Tearney, C. C. Compton, and N. S. Nishioka, “Optical coherence tomography in the gastrointestinal tract,” Endoscopy 32(10), 796–803 (2000).
[Crossref] [PubMed]

N. D. Gladkova, G. A. Petrova, N. K. Nikulin, S. G. Radenska-Lopovok, L. B. Snopova, Y. P. Chumakov, V. A. Nasonova, V. M. Gelikonov, G. V. Gelikonov, R. V. Kuranov, A. M. Sergeev, and F. I. Feldchtein, “In vivo optical coherence tomography imaging of human skin: norm and pathology,” Skin Res. Technol. 6(1), 6–16 (2000).
[Crossref] [PubMed]

1998 (2)

F. G. Holz, C. Bellmann, K. Rohrschneider, R. O. Burk, and H. E. Völcker, “Simultaneous confocal scanning laser fluorescein and indocyanine green angiography,” Am. J. Ophthalmol. 125(2), 227–236 (1998).
[Crossref] [PubMed]

G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
[Crossref] [PubMed]

1996 (2)

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59(3), 427–471 (1996).
[Crossref]

A. F. Fercher, “Optical coherence tomography,” J. Biomed. Opt. 1(2), 157–173 (1996).
[Crossref] [PubMed]

1993 (1)

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

1989 (1)

M. Boulton, N. M. McKechnie, J. Breda, M. Bayly, and J. Marshall, “The formation of autofluorescent granules in cultured human RPE,” Invest. Ophthalmol. Vis. Sci. 30(1), 82–89 (1989).
[PubMed]

1976 (1)

G. De Venecia, M. Davis, and R. Engerman, “Clinicopathologic correlations in diabetic retinopathy. I. Histology and fluorescein angiography of microaneurysms,” Arch. Ophthalmol. 94(10), 1766–1773 (1976).
[Crossref] [PubMed]

An, L.

Applegate, B. E.

Balas, C.

C. Balas, “Review of biomedical optical imaging—a powerful, non-invasive, non-ionizing technology for improving in vivo diagnosis,” Meas. Sci. Technol. 20(10), 104020 (2009).
[Crossref]

Bauer-Marschallinger, J.

T. Berer, E. Leiss-Holzinger, A. Hochreiner, J. Bauer-Marschallinger, and A. Buchsbaum, “Multimodal noncontact photoacoustic and optical coherence tomography imaging using wavelength-division multiplexing,” J. Biomed. Opt. 20(4), 46013 (2015).
[Crossref] [PubMed]

Bayly, M.

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Figures (5)

Fig. 1
Fig. 1 Schematic of the integrated PAM/OCT/ODT/CFM experimental system. SLD: Superluminescent diode; FC: 2 × 2 Fiber coupler; PC: Polarization controller; L1, L2, L3, L4: Lens; M1, M2, M3: Mirror; DM1, DM2: Dichroic mirror; C1, C2, C3: Collimator; ND: Neutral density filter; F1, F2, F3: Optical filter; PBS: Pellicle beam splitter; PD: Photodiode.
Fig. 2
Fig. 2 Measured optical spectrum of the pulsed laser before and after the single-mode optical fibers. (a) laser spectrum before the optical fiber; (b) laser spectrum exiting a 4.5 m long single-mode optical fiber; (c) laser spectrum exiting a 0.5 m long single-mode optical fiber. The intensity readings are normalized.
Fig. 3
Fig. 3 Phantom test of OCT-guided dynamic focusing using surface contour scanning. (a) OCT B-scan at the location marked in panel (e) as a yellow line; (b) OCT B-scan of the angled plate; (c) and (d) Simultaneously acquired PAM and CFM images without dynamic focusing; (e) and (f) Simultaneously acquired PAM and CFM images with dynamic focusing; (g) PA signal intensity along the line at the location marked in panel (c) and (e) as a red and blue line without and with dynamic focusing, respectively; (h) FL (fluorescence) signal intensity along the line at the location marked in panel (d) and (f) as a red and blue line without and with dynamic focusing, respectively; bar: 100μm.
Fig. 4
Fig. 4 Multimodal imaging of a human eye ex vivo using OCT-guided dynamic focusing. (a) and (b) Simultaneously acquired PAM and CFM images without dynamic focusing; (c) and (d) Simultaneously acquired PAM and CFM images with dynamic focusing; (e) OCT B-scan at the location marked in panel (a) by the yellow solid line (displayed dynamic range, 55 dB); (f) PA signal intensity along the line at the location marked in panel (a) and (c) as a red and blue line without and with dynamic focusing, respectively; (g) FL (fluorescence) signal intensity along the line at the location marked in panel (b) and (d) as a red and blue line without and with dynamic focusing, respectively; RPE: Retinal Pigment Epithelium; SL: Sclera; bar, 500 μm.
Fig. 5
Fig. 5 Simultaneously acquired PAM, CFM, OCT and ODT images of a mouse ear with dynamic focusing. (a) PA image (average contrast-to-noise ratio 50 dB); (b) OCT B-scan at the location marked in panel (e) by the solid line (displayed dynamic range, 45 dB); (c) ODT B-scan at the location marked in panel (e) by the solid line; (d) CFM image (average contrast-to-noise ratio 30 dB); (e) OCT 2D projection images generated from the acquired 3D OCT data sets; (f) Fused 2D image of simultaneously acquired PAM, CFM and OCT images; SG: Sebaceous glands; bar, 100μm.

Equations (1)

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v p = Δ φ i λ 0 f Aline 4 πn ,

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