A fast all-optical 3D photoacoustic scanner for clinical vascular imaging
Language English Country England, Great Britain Media print-electronic
Document type Journal Article
Grant support
Wellcome Trust - United Kingdom
PubMed
39349585
PubMed Central
PMC12092260
DOI
10.1038/s41551-024-01247-x
PII: 10.1038/s41551-024-01247-x
Knihovny.cz E-resources
- MeSH
- Skin blood supply MeSH
- Humans MeSH
- Microvessels diagnostic imaging MeSH
- Photoacoustic Techniques * methods instrumentation MeSH
- Arthritis, Rheumatoid diagnostic imaging MeSH
- Imaging, Three-Dimensional * methods instrumentation MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
The clinical assessment of microvascular pathologies (in diabetes and in inflammatory skin diseases, for example) requires the visualization of superficial vascular anatomy. Photoacoustic tomography (PAT) scanners based on an all-optical Fabry-Perot ultrasound sensor can provide highly detailed 3D microvascular images, but minutes-long acquisition times have precluded their clinical use. Here we show that scan times can be reduced to a few seconds and even hundreds of milliseconds by parallelizing the optical architecture of the sensor readout, by using excitation lasers with high pulse-repetition frequencies and by exploiting compressed sensing. A PAT scanner with such fast acquisition minimizes motion-related artefacts and allows for the volumetric visualization of individual arterioles, venules, venous valves and millimetre-scale arteries and veins to depths approaching 15 mm, as well as for dynamic 3D images of time-varying tissue perfusion and other haemodynamic events. In exploratory case studies, we used the scanner to visualize and quantify microvascular changes associated with peripheral vascular disease, skin inflammation and rheumatoid arthritis. Fast all-optical PAT may prove useful in cardiovascular medicine, oncology, dermatology and rheumatology.
Centrum Wiskunde and Informatica Amsterdam the Netherlands
Department of Computer Science University College London London UK
Department of Medical Physics and Biomedical Engineering University College London London UK
Faculty of Information Technology Brno University of Technology Brno Czech Republic
Imperial College Healthcare NHS Trust London UK
University College London Hospital NHS Foundation Trust London UK
Wellcome EPSRC Centre for Interventional and Surgical Sciences University College London London UK
See more in PubMed
James, W. D., Elston, D., Treat, J. R. & Rosenbach, M. A. Andrews’ Diseases of the Skin: Clinical Dermatology 13th edn (Elsevier, 2019).
Chao, C. Y. L. & Cheing, G. L. Y. Microvascular dysfunction in diabetic foot disease and ulceration. Diabetes Metab. Res. Rev.25, 604–614 (2009). PubMed
Paul, D. W. et al. Noninvasive imaging technologies for cutaneous wound assessment: a review. Wound Repair Regen.23, 149–162 (2015). PubMed
Allen, J. & Howell, K. Microvascular imaging: techniques and opportunities for clinical physiological measurements. Physiol. Meas.35, R91–R141 (2014). PubMed
Deegan, A. J. & Wang, R. K. Microvascular imaging of the skin. Phys. Med. Biol.64, 07TR01 (2019). PubMed PMC
Tanter, M. & Fink, M. Ultrafast imaging in biomedical ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control61, 102–119 (2014). PubMed
Soloukey, S. et al. Functional ultrasound (fUS) during awake brain surgery: the clinical potential of intra-operative functional and vascular brain mapping. Front. Neurosci.13, 1384 (2020). PubMed PMC
Beard, P. Biomedical photoacoustic imaging. Interface Focus1, 602–631 (2011). PubMed PMC
Su, R., Ermilov, S., Liopo, A. & Oraevsky, A. Laser optoacoustic tomography: towards new technology for biomedical diagnostics. Nucl. Instrum. Methods Phys. Res. A720, 58–61 (2013). PubMed PMC
Wang, L. V. & Yao, J. A practical guide to photoacoustic tomography in the life sciences. Nat. Methods13, 627–638 (2016). PubMed PMC
Taruttis, A., van Dam, G. M. & Ntziachristos, V. Mesoscopic and macroscopic optoacoustic imaging of cancer. Cancer Res.75, 1548–1559 (2015). PubMed
Li, D., Humayun, L., Vienneau, E., Vu, T. & Yao, J. Seeing through the skin: photoacoustic tomography of skin vasculature and beyond. JID Innov.1, 100039 (2021). PubMed PMC
Li, M., Tang, Y. & Yao, J. Photoacoustic tomography of blood oxygenation: a mini review. Photoacoustics10, 65–73 (2018). PubMed PMC
Lin, L. & Wang, L. V. The emerging role of photoacoustic imaging in clinical oncology. Nat. Rev. Clin. Oncol.19, 365–384 (2022). PubMed
Valluru, K. S., Wilson, K. E. & Willmann, J. K. Photoacoustic imaging in oncology: translational preclinical and early clinical experience. Radiology280, 332–349 (2016). PubMed PMC
Karlas, A. et al. Cardiovascular optoacoustics: from mice to men – a review. Photoacoustics14, 19–30 (2019). PubMed PMC
Karlas, A. et al. Multispectral optoacoustic tomography of peripheral arterial disease based on muscle hemoglobin gradients—a pilot clinical study. Ann. Transl. Med.9, 36–36 (2021). PubMed PMC
Yang, J. et al. Detecting hemodynamic changes in the foot vessels of diabetic patients by photoacoustic tomography. J. Biophotonics13, e202000011 (2020). PubMed
Karlas, A. et al. Dermal features derived from optoacoustic tomograms via machine learning correlate microangiopathy phenotypes with diabetes stage. Nat. Biomed. Eng.7, 1667–1682 (2023). PubMed PMC
Zabihian, B. et al. In vivo dual-modality photoacoustic and optical coherence tomography imaging of human dermatological pathologies. Biomed. Opt. Express6, 3163–3178 (2015). PubMed PMC
van den Berg, P. J., Daoudi, K., Bernelot Moens, H. J. & Steenbergen, W. Feasibility of photoacoustic/ultrasound imaging of synovitis in finger joints using a point-of-care system. Photoacoustics8, 8–14 (2017). PubMed PMC
Jo, J. et al. Photoacoustic tomography for human musculoskeletal imaging and inflammatory arthritis detection. Photoacoustics12, 82–89 (2018). PubMed PMC
Rajian, J. R., Shao, X., Chamberland, D. L. & Wang, X. Characterization and treatment monitoring of inflammatory arthritis by photoacoustic imaging: a study on adjuvant-induced arthritis rat model. Biomed. Opt. Express4, 900–908 (2013). PubMed PMC
Nam, S. Y., Chung, E., Suggs, L. J. & Emelianov, S. Y. Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct. Tissue Eng. C Methods21, 557–566 (2015). PubMed PMC
Mantri, Y., Mishra, A., Anderson, C. A. & Jokerst, J. V. Photoacoustic imaging to monitor outcomes during hyperbaric oxygen therapy: validation in a small cohort and case study in a bilateral chronic ischemic wound. Biomed. Opt. Express13, 5683–5694 (2022). PubMed PMC
Deán-Ben, X. L. & Razansky, D. Portable spherical array probe for volumetric real-time optoacoustic imaging at centimeter-scale depths. Opt. Express21, 28062–28071 (2013). PubMed
Zhang, H. F., Maslov, K., Stoica, G. & Wang, L. V. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat. Biotechnol.24, 848–851 (2006). PubMed
Aguirre, J. et al. Precision assessment of label-free psoriasis biomarkers with ultra-broadband optoacoustic mesoscopy. Nat. Biomed. Eng.1, 0068 (2017).
Tadayon, M. A., Baylor, M. & Ashkenazi, S. Polymer waveguide Fabry–Perot resonator for high-frequency ultrasound detection. IEEE Trans. Ultrason. Ferroelectr. Freq. Control61, 2132–2138 (2014). PubMed
Preisser, S. et al. All-optical highly sensitive akinetic sensor for ultrasound detection and photoacoustic imaging. Biomed. Opt. Express7, 4171–4186 (2016). PubMed PMC
Hajireza, P., Krause, K., Brett, M. & Zemp, R. Glancing angle deposited nanostructured film Fabry–Perot etalons for optical detection of ultrasound. Opt. Express21, 6391–6400 (2013). PubMed
Guggenheim, J. A. et al. Ultrasensitive plano-concave optical microresonators for ultrasound sensing. Nat. Photonics11, 714–719 (2017).
Li, H., Dong, B., Zhang, Z., Zhang, H. F. & Sun, C. A transparent broadband ultrasonic detector based on an optical micro-ring resonator for photoacoustic microscopy. Sci. Rep.4, 4496 (2014). PubMed PMC
Shnaiderman, R. et al. A submicrometre silicon-on-insulator resonator for ultrasound detection. Nature585, 372–378 (2020). PubMed
Westerveld, W. J. et al. Sensitive, small, broadband and scalable optomechanical ultrasound sensor in silicon photonics. Nat. Photonics15, 341–345 (2021).
Harary, T., Hazan, Y. & Rosenthal, A. All-optical optoacoustic micro-tomography in reflection mode. Biomed. Eng. Lett.13, 475–483 (2023). PubMed PMC
Zhang, E., Laufer, J. & Beard, P. Backward-mode multiwavelength photoacoustic scanner using a planar Fabry–Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues. Appl. Opt.47, 561–577 (2008). PubMed
Laufer, J. et al. In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy. J. Biomed. Opt.17, 056016 (2012). PubMed
Johnson, S. P., Ogunlade, O., Lythgoe, M. F., Beard, P. & Pedley, R. B. Longitudinal photoacoustic imaging of the pharmacodynamic effect of vascular targeted therapy on tumors. Clin. Cancer Res.25, 7436–7448 (2019). PubMed PMC
Ogunlade, O. et al. In vivo three-dimensional photoacoustic imaging of the renal vasculature in preclinical rodent models. Am. J. Physiol. Ren. Physiol.314, F1145–F1153 (2018). PubMed
Huynh, N., Ogunlade, O., Zhang, E., Cox, B. & Beard, P. Photoacoustic imaging using an 8-beam Fabry–Perot scanner>. In Proc. SPIE 9708, Photons Plus Ultrasound (eds Oraevsky, A. A. & Wang, L. V.) 97082L (SPIE, 2016).
Plumb, A. A., Huynh, N. T., Guggenheim, J., Zhang, E. & Beard, P. Rapid volumetric photoacoustic tomographic imaging with a Fabry–Perot ultrasound sensor depicts peripheral arteries and microvascular vasomotor responses to thermal stimuli. Eur. Radiol.28, 1037–1045 (2018). PubMed PMC
Jathoul, A. P. et al. Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinase-based genetic reporter. Nat. Photonics9, 239–246 (2015).
Märk, J. et al. Dual-wavelength 3D photoacoustic imaging of mammalian cells using a photoswitchable phytochrome reporter protein. Commun. Phys.1, 3 (2018).
Ma, X., Fan, M., Cai, Y., Xu, L. & Ma, J. A Fabry–Perot fiber-optic array for photoacoustic imaging. IEEE Trans. Instrum. Meas.71, 4501508 (2022).
Saucourt, J., Moreau, A., Lumeau, J., Rigneault, H. & Chaigne, T. Fast interrogation wavelength tuning for all-optical photoacoustic imaging. Opt. Express31, 11164–11172 (2023). PubMed
Cox, B. T. & Beard, P. C. The frequency-dependent directivity of a planar Fabry–Perot polymer film ultrasound sensor. IEEE Trans. Ultrason. Ferroelectr. Freq. Control54, 394–404 (2007). PubMed
Morris, P., Hurrell, A., Shaw, A., Zhang, E. & Beard, P. A Fabry–Pérot fiber-optic ultrasonic hydrophone for the simultaneous measurement of temperature and acoustic pressure. J. Acoust. Soc. Am.125, 3611–3622 (2009). PubMed
Allen, T. J. et al. High pulse energy fibre laser as an excitation source for photoacoustic tomography. Opt. Express28, 34255–34265 (2020). PubMed
Arridge, S. R. et al. Accelerated high-resolution photoacoustic tomography via compressed sensing. Phys. Med. Biol.61, 8908–8940 (2016). PubMed
Köstli, K. P., Frenz, M., Bebie, H. & Weber, H. P. Temporal backward projection of optoacoustic pressure transients using Fourier transform methods. Phys. Med. Biol.46, 1863–1872 (2001). PubMed
Caggiati, A., Phillips, M., Lametschwandtner, A. & Allegra, C. Valves in small veins and venules. Eur. J. Vasc. Endovasc. Surg.32, 447–452 (2006). PubMed
Pu, K. et al. Semiconducting polymer nanoparticles as photoacoustic molecular imaging probes in living mice. Nat. Nanotechnol.9, 233–239 (2014). PubMed PMC
De Angelis, R., Grassi, W. & Cutolo, M. A growing need for capillaroscopy in rheumatology. Arthritis Rheum.61, 405–410 (2009). PubMed
Ingegnoli, F. et al. Prognostic model based on nailfold capillaroscopy for identifying Raynaud’s phenomenon patients at high risk for the development of a scleroderma spectrum disorder: PRINCE (Prognostic Index for Nailfold Capillaroscopic Examination). Arthritis Rheum.58, 2174–2182 (2008). PubMed
Haltmeier et al. Compressed sensing and sparsity in photoacoustic tomography. J. Opt.18, 114004–114012 (2016).
Antholzer, S., Haltmeier, M. & Schwab, J. Deep learning for photoacoustic tomography from sparse data. Inverse Prob. Sci. Eng.27, 987–1005 (2019). PubMed PMC
Davoudi, N., Deán-Ben, X. L. & Razansky, D. Deep learning optoacoustic tomography with sparse data. Nat. Mach. Intell.1, 453–460 (2019).
Özbek, A., Deán-Ben, X. L. & Razansky, D. Optoacoustic imaging at kilohertz volumetric frame rates. Optica5, 857–863 (2018). PubMed PMC
Hauptmann, A. & Cox, B. Deep learning in photoacoustic tomography: current approaches and future directions. J. Biomed. Opt.25, 112903 (2020).
Pan, B. & Betcke, M. M. On learning the invisible in photoacoustic tomography with flat directionally sensitive detector. SIAM J. Imag. Sci.16, 770–801 (2023).
Roustit, M. & Cracowski, J.-L. Assessment of endothelial and neurovascular function in human skin microcirculation. Trends Pharmacol. Sci.34, 373–384 (2013). PubMed
Rossi, M. et al. Peripheral microvascular dysfunction as an independent predictor of atherosclerotic damage in type 1 diabetes patients: a preliminary study. Clin. Hemorheol. Microcirc.54, 381–391 (2013). PubMed
Belch, J. J. et al. Critical issues in peripheral arterial disease detection and management: a call to action. Arch. Intern. Med.163, 884–892 (2003). PubMed
Han, H.-C. C. Twisted blood vessels: symptoms, etiology and biomechanical mechanisms. J. Vasc. Res.49, 185–197 (2012). PubMed PMC
Owen, C. G. et al. Diabetes and the tortuosity of vessels of the bulbar conjunctiva. Ophthalmology115, e27–e32 (2008). PubMed
Ciurică, S. et al. Arterial tortuosity. Hypertension73, 951–960 (2019). PubMed
Almutairi, K. B., Nossent, J. C., Preen, D. B., Keen, H. I. & Inderjeeth, C. A. The prevalence of rheumatoid arthritis: a systematic review of population-based Studies. J. Rheumatol.48, 669–676 (2021). PubMed
Wiacek, A. & Lediju Bell, M. A. Photoacoustic-guided surgery from head to toe [Invited]. Biomed. Opt. Express12, 2079–2117 (2021). PubMed PMC
Ansari, R., Zhang, E. Z., Desjardins, A. E. & Beard, P. C. All-optical forward-viewing photoacoustic probe for high-resolution 3D endoscopy. Light. Sci. Appl.7, 75 (2018). PubMed PMC
Ansari, R., Zhang, E., Desjardins, A. & Beard, P. Miniature all-optical flexible forward-viewing photoacoustic endoscopy probe for surgical guidance. Opt. Lett.45, 6238–6241 (2020). PubMed PMC
Ansari, R., Zhang, E. & Beard, P. Dual-modality rigid endoscope for photoacoustic imaging and white light videoscopy. J. Biomed. Opt.29, 020502 (2024). PubMed PMC
Lamont, M. & Beard, P. 2D imaging of ultrasound fields using CCD array to map output of Fabry–Perot polymer film sensor. Electron. Lett.42, 7–8 (2006).
Sievers, J., Villringer, C., Lebek, W., Gilani, T. & Laufer, J. Photoacoustic tomography using a Fabry–Perot sensor with homogeneous optical thickness and wide-field camera-based detection. In Opto-Acoustic Methods and Applications in Biophotonics VI (eds Zemp, R. J. et al.) 126310P (SPIE, 2023).
Zhang, E. Z. & Beard, P. C. A miniature all-optical photoacoustic imaging probe. In Proc. SPIE, Photons Plus Ultrasound Vol. 7899 (eds Oraevsky, A. A. & Wang, L. V.) 78991F (SPIE, 2011).
Zhang, E. Z. et al. Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging. Biomed. Opt. Express2, 2202–2215 (2011). PubMed PMC
Pham, K. et al. Broadband all-optical plane-wave ultrasound imaging system based on a Fabry–Perot scanner. IEEE Trans. Ultrason. Ferroelectr. Freq. Control68, 1007–1016 (2021). PubMed
Yasuda, H. Plasma Polymerisation (Academic Press, 1985).
Treeby, B. E., Jaros, J. & Cox, B. T. Advanced photoacoustic image reconstruction using the k-Wave toolbox. In Proc. SPIE, Photons Plus Ultrasound Vol. 9708 (eds Oraevsky, A. A. & Wang, L. V.) 97082P (SPIE, 2016).
Treeby, B. E., Varslot, T. K., Zhang, E. Z., Laufer, J. G. & Beard, P. C. Automatic sound speed selection in photoacoustic image reconstruction using an autofocus approach. J. Biomed. Opt.16, 090501 (2011). PubMed
Treeby, B. E. & Cox, B. T. k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields. J. Biomed. Opt.15, 021314 (2010). PubMed
Arthur, D. & Vassilvitskii, S. K-means++: the advantages of careful seeding. In Proc. 18th Annual ACM-SIAM Symposium on Discrete Algorithms 1027–1035 (Society for Industrial and Applied Mathematics, 2007).