• Advanced Imaging
  • Vol. 1, Issue 3, 032002 (2024)
Junho Ahn1,†, Minseong Kim1, Chulhong Kim1,2,*, and Wonseok Choi3,*
Author Affiliations
  • 1Department of Convergence IT Engineering, Electrical Engineering, Mechanical Engineering, and Medical Science and Engineering, Pohang University of Science and Technology, Pohang, Republic of Korea
  • 2Opticho Inc., Pohang, Republic of Korea
  • 3Department of Biomedical Engineering and Medical Sciences, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
  • show less
    DOI: 10.3788/AI.2024.20005 Cite this Article Set citation alerts
    Junho Ahn, Minseong Kim, Chulhong Kim, Wonseok Choi, "In vivo multi-scale clinical photoacoustic imaging for analysis of skin vasculature and pigmentation: a comparative review," Adv. Imaging 1, 032002 (2024) Copy Citation Text show less
    References

    [1] A. G. Bell. The photophone. J. Franklin Inst., 110, 237(1880).

    [2] Y. Fan et al. Development of a laser photothermoacoustic frequency-swept system for subsurface imaging: theory and experiment. J. Acoust. Soc. Am., 116, 3523(2004).

    [3] M. Xu, L. V. Wang. Photoacoustic imaging in biomedicine. Rev. Sci. Instrum., 77, 041101(2006).

    [4] S. Takatani, M. D. Graham. Theoretical analysis of diffuse reflectance from a two-layer tissue model. IEEE Trans. Biomed. Eng., BME-26, 656(1979).

    [5] S. L. Jacques, R. D. Glickman, J. A. Schwartz. Internal absorption coefficient and threshold for pulsed laser disruption of melanosomes isolated from retinal pigment epithelium. Proc. SPIE, 2681, 468(1996).

    [6] J. B. Dawson et al. A theoretical and experimental study of light absorption and scattering by in vivo skin. Phys. Med. Biol., 25, 695(1980).

    [7] S. H. Tseng et al. Chromophore concentrations, absorption and scattering properties of human skin in-vivo. Opt. Express, 17, 14599(2009).

    [8] S. Choi et al. X-ray free-electron laser induced acoustic microscopy (XFELAM). Photoacoustics, 35, 100587(2024).

    [9] D. Kim et al. An ultraviolet-transparent ultrasound transducer enables high-resolution label-free photoacoustic histopathology. Laser Photonics Rev., 18, 2300652(2024).

    [10] J. Laufer et al. 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, 141(2007).

    [11] B. Park et al. Functional photoacoustic imaging: from nano- and micro- to macro-scale. Nano Converg., 10, 29(2023).

    [12] C. Cano et al. Deep learning assisted classification of spectral photoacoustic imaging of carotid plaques. Photoacoustics, 33, 100544(2023).

    [13] C. Kim et al. In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. ACS Nano, 4, 4559(2010).

    [14] W. Choi et al. Recent advances in contrast-enhanced photoacoustic imaging: overcoming the physical and practical challenges. Chem. Rev., 123, 7379(2023).

    [15] B. Park et al. Listening to drug delivery and responses via photoacoustic imaging. Adv. Drug Deliv. Rev., 184, 114235(2022).

    [16] R. Gao et al. Background-suppressed tumor-targeted photoacoustic imaging using bacterial carriers. Proc. Natl. Acad. Sci. U.S.A., 119, e2121982119(2022).

    [17] R. Gao et al. Nonlinear mechanisms in photoacoustics—powerful tools in photoacoustic imaging. Photoacoustics, 22, 100243(2021).

    [18] R. Gao et al. Breaking acoustic limit of optical focusing using photoacoustic-guided wavefront shaping. Laser Photonics Rev., 15, 2000594(2021).

    [19] Z. Huang et al. Multimodal PA/US imaging in rheumatoid arthritis: enhanced correlation with clinical scores. Photoacoustics, 38, 100615(2024).

    [20] S. Wang et al. Tri-modality in vivo imaging for tumor detection with combined ultrasound, photoacoustic, and photoacoustic elastography. Photoacoustics, 38, 100630(2024).

    [21] A. P. Träger et al. Hybrid ultrasound and single wavelength optoacoustic imaging reveals muscle degeneration in peripheral artery disease. Photoacoustics, 35, 100579(2024).

    [22] Y. Yu et al. Simultaneous photoacoustic and ultrasound imaging: a review. Ultrasonics, 139, 107277(2024).

    [23] X. Mu et al. On-demand expansion fluorescence and photoacoustic microscopy (ExFLPAM). Photoacoustics, 38, 100610(2024).

    [24] J. Park et al. Quadruple ultrasound, photoacoustic, optical coherence, and fluorescence fusion imaging with a transparent ultrasound transducer. Proc. Natl. Acad. Sci. U.S.A., 118, e1920879118(2021).

    [25] X. Wei et al. Deep learning-powered biomedical photoacoustic imaging. Neurocomputing, 573, 127207(2024).

    [26] H. Zhao et al. Deep learning enables superior photoacoustic imaging at ultralow laser dosages. Adv. Sci., 8, 2003097(2021).

    [27] X. Zhu et al. Real-time whole-brain imaging of hemodynamics and oxygenation at micro-vessel resolution with ultrafast wide-field photoacoustic microscopy. Light Sci. Appl., 11, 138(2022).

    [28] X. Yang et al. Photoacoustic imaging for monitoring of stroke diseases: a review. Photoacoustics, 23, 100287(2021).

    [29] R. Cao et al. Photoacoustic microscopy reveals the hemodynamic basis of sphingosine 1-phosphate-induced neuroprotection against ischemic stroke. Theranostics, 8, 6111(2018).

    [30] Z. Chen et al. Multimodal noninvasive functional neurophotonic imaging of murine brain-wide sensory responses. Adv. Sci., 9, 2105588(2022).

    [31] V. Tsytsarev et al. Photoacoustic microscopy of microvascular responses to cortical electrical stimulation. J. Biomed. Opt., 16, 1(2011).

    [32] W. Liu et al. In vivo corneal neovascularization imaging by optical-resolution photoacoustic microscopy. Photoacoustics, 2, 81(2014).

    [33] S. Hu et al. Label-free photoacoustic ophthalmic angiography. Opt. Lett., 35, 1(2010).

    [34] W. Liu, H. F. Zhang. Photoacoustic imaging of the eye: a mini review. Photoacoustics, 4, 112(2016).

    [35] S. Jiao et al. Photoacoustic ophthalmoscopy for in vivo retinal imaging. Opt. Express, 18, 3967(2010).

    [36] D. Kim et al. In vivo quantitative photoacoustic monitoring of corticosteroid-induced vasoconstriction. J. Biomed. Opt., 28, 082805(2023).

    [37] A. B. E. Attia et al. A review of clinical photoacoustic imaging: current and future trends. Photoacoustics, 16, 100144(2019).

    [38] E. Y. Park et al. Photoacoustic imaging systems based on clinical ultrasound platform. Exp. Biol. Med., 247, 551(2022).

    [39] H. Assi et al. A review of a strategic roadmapping exercise to advance clinical translation of photoacoustic imaging: from current barriers to future adoption. Photoacoustics, 32, 100539(2023).

    [40] V. S. Dogra et al. Preliminary results of ex vivo multispectral photoacoustic imaging in the management of thyroid cancer. AJR Am. J. Roentgenol., 202, W552(2014).

    [41] A. Dima, V. Ntziachristos. In-vivo handheld optoacoustic tomography of the human thyroid. Photoacoustics, 4, 65(2016).

    [42] M. Yang et al. Photoacoustic/ultrasound dual imaging of human thyroid cancers: an initial clinical study. Biomed Opt. Express, 8, 3449(2017).

    [43] J. Kim et al. Multiparametric photoacoustic analysis of human thyroid cancers in vivo. Cancer Res., 81, 4849(2021).

    [44] B. Park, C. Kim, J. Kim. Recent advances in ultrasound and photoacoustic analysis for thyroid cancer diagnosis. Adv. Phys. Res., 2, 2200070(2023).

    [45] M. Toi et al. Visualization of tumor-related blood vessels in human breast by photoacoustic imaging system with a hemispherical detector array. Sci. Rep., 7, 41970(2017).

    [46] G. Diot et al. Multispectral optoacoustic tomography (MSOT) of human breast cancer. Clin. Cancer Res., 23, 6912(2017).

    [47] E. I. Neuschler et al. A pivotal study of optoacoustic imaging to diagnose benign and malignant breast masses: a new evaluation tool for radiologists. Radiology, 287, 398(2018).

    [48] A. Karlas et al. Cardiovascular optoacoustics: from mice to men - a review. Photoacoustics, 14, 19(2019).

    [49] M. Wu et al. Emerging technology update intravascular photoacoustic imaging of vulnerable atherosclerotic plaque. Interv. Cardiol., 11, 120(2016).

    [50] K. Jansen, G. van Soest, A. F. W. van der Steen. Intravascular photoacoustic imaging: a new tool for vulnerable plaque identification. Ultrasound Med. Biol., 40, 1037(2014).

    [51] H. Zafar et al. Photoacoustic cardiovascular imaging: a new technique for imaging of atherosclerosis and vulnerable plaque detection. Biomed. Phys. Eng. Express, 4, 032002(2018).

    [52] W. Choi et al. Three-dimensional multistructural quantitative photoacoustic and US imaging of human feet in vivo. Radiology, 303, 467(2022).

    [53] J. Yang et al. Detecting hemodynamic changes in the foot vessels of diabetic patients by photoacoustic tomography. J. Biophotonics, 13, e202000011(2020).

    [54] S. Nemirova et al. Scanning optoacoustic angiography for assessing structural and functional alterations in superficial vasculature of patients with post-thrombotic syndrome: a pilot study. Photoacoustics, 38, 100616(2024).

    [55] T. Chen et al. Dedicated photoacoustic imaging instrument for human periphery blood vessels: a new paradigm for understanding the vascular health. IEEE Trans. Biomed. Eng., 69, 1093(2022).

    [56] J. Ahn et al. High-resolution functional photoacoustic monitoring of vascular dynamics in human fingers. Photoacoustics, 23, 100282(2021).

    [57] R. Huggenberger, M. Detmar. The cutaneous vascular system in chronic skin inflammation. J. Investig. Dermatol Symp. Proc., 15, 24(2011).

    [58] M. Lupu et al. Vascular patterns in basal cell carcinoma: dermoscopic, confocal and histopathological perspectives. Oncol. Lett., 17, 4112(2019).

    [59] H. R. Moreira, A. P. Marques. Vascularization in skin wound healing: where do we stand and where do we go?. Curr. Opin. Biotechnol., 73, 253(2022).

    [60] P. Mabeta. Paradigms of vascularization in melanoma: clinical significance and potential for therapeutic targeting. Biomed. Pharmacother., 127, 110135(2020).

    [61] S. Gupta et al. Dermal vasculature in psoriasis and psoriasiform dermatitis: a morphometric study. Indian J. Dermatol., 56, 647(2011).

    [62] R. Waelchli et al. New vascular classification of port-wine stains: improving prediction of Sturge-Weber risk. Br. J. Dermatol., 171, 861(2014).

    [63] M. Steinhoff et al. Role of vasculature in atopic dermatitis. J. Allergy Clin. Immunol., 118, 190(2006).

    [64] A. W. Barrett, A. D. Beynon. A histochemical study on the distribution of melanin in human oral epithelium at six regional sites. Arch. Oral Biol., 36, 771(1991).

    [65] G. T. Pack, N. Lenson, D. M. Gerber. Regional distribution of moles and melanomas. AMA Arch. Surg., 65, 862(1952).

    [66] Y. Zhang et al. Chronic label-free volumetric photoacoustic microscopy of melanoma cells in three-dimensional porous scaffolds. Biomaterials, 31, 8651(2010).

    [67] K. Abhishek, N. Khunger. Complications of skin biopsy. J. Cutan. Aesthet. Surg., 8, 239(2015).

    [68] D. Oh et al. Contrast agent-free 3D renal ultrafast doppler imaging reveals vascular dysfunction in acute and diabetic kidney diseases. Adv. Sci., 10, 2303966(2023).

    [69] S. Cho et al. An ultrasensitive and broadband transparent ultrasound transducer for ultrasound and photoacoustic imaging in-vivo. Nat. Commun., 15, 1444(2024).

    [70] S. Jeon et al. A novel 2-D synthetic aperture focusing technique for acoustic-resolution photoacoustic microscopy. IEEE Trans. Med. Imaging, 38, 250(2019).

    [71] H. Zhao et al. Motion correction in optical resolution photoacoustic microscopy. IEEE Trans. Med. Imaging, 38, 2139(2019).

    [72] H. Zhao et al. Three-dimensional Hessian matrix-based quantitative vascular imaging of rat iris with optical-resolution photoacoustic microscopy in vivo. J. Biomed Opt., 23, 1(2018).

    [73] J. Meng et al. WSA-MP-Net: weak-signal-attention and multi-scale perception network for microvascular extraction in optical-resolution photoacoustic microcopy. Photoacoustics, 37, 100600(2024).

    [74] C. Yoon et al. Deep learning-based virtual staining, segmentation, and classification in label-free photoacoustic histology of human specimens. Light Sci. Appl., 13, 226(2024).

    [75] H. Lee et al. Transportable multispectral optical-resolution photoacoustic microscopy using stimulated Raman scattering spectrum. IEEE Trans. Instrum. Meas., 73, 4502309(2024).

    [76] J. Ahn et al. In vivo photoacoustic monitoring of vasoconstriction induced by acute hyperglycemia. Photoacoustics, 30, 100485(2023).

    [77] J. Chen et al. Wide-field polygon-scanning photoacoustic microscopy of oxygen saturation at 1-MHz A-line rate. Photoacoustics, 20, 100195(2020).

    [78] R. Shintate et al. High-speed optical resolution photoacoustic microscopy with MEMS scanner using a novel and simple distortion correction method. Sci. Rep., 12, 9221(2022).

    [79] J. W. Baik et al. Super wide-field photoacoustic microscopy of animals and humans in vivo. IEEE Trans. Med. Imaging, 39, 975(2020).

    [80] M. Zafar et al. Ultra-widefield and high-speed spiral laser scanning OR-PAM: system development and characterization. J. Biophotonics, 16, e202200383(2023).

    [81] Z. Xie et al. Laser-scanning optical-resolution photoacoustic microscopy. Opt. Lett., 34, 1771(2009).

    [82] J. Kim et al. Deep learning acceleration of multiscale superresolution localization photoacoustic imaging. Light Sci. Appl., 11, 131(2022).

    [83] N. Chen et al. Video-rate high-resolution single-pixel nonscanning photoacoustic microscopy. Biomed. Opt. Express, 13, 3823(2022).

    [84] U. A. T. Hofmann et al. Enhancing optoacoustic mesoscopy through calibration-based iterative reconstruction. Photoacoustics, 28, 100405(2022).

    [85] J. Aguirre et al. Precision assessment of label-free psoriasis biomarkers with ultra-broadband optoacoustic mesoscopy. Nat. Biomed. Eng., 1, 0068(2017).

    [86] S. Cho et al. 3D PHOVIS: 3D photoacoustic visualization studio. Photoacoustics, 18, 100168(2020).

    [87] W. Kim et al. Wide-field three-dimensional photoacoustic/ultrasound scanner using a two-dimensional matrix transducer array. Opt. Lett., 48, 343(2023).

    [88] R. A. Kruger et al. Dedicated 3D photoacoustic breast imaging. Med. Phys., 40, 113301(2013).

    [89] J. Yang, S. Choi, C. Kim. Practical review on photoacoustic computed tomography using curved ultrasound array transducer. Biomed. Eng. Lett., 12, 19(2022).

    [90] C. Lee, C. Kim, B. Park. Review of three-dimensional handheld photoacoustic and ultrasound imaging systems and their applications. Sensors, 23, 8149(2023).

    [91] C. Lee et al. Panoramic volumetric clinical handheld photoacoustic and ultrasound imaging. Photoacoustics, 31, 100512(2023).

    [92] R. Gao et al. Restoring the imaging quality of circular transducer array-based PACT using synthetic aperture focusing technique integrated with 2nd-derivative-based back projection scheme. Photoacoustics, 32, 100537(2023).

    [93] S. Choi et al. Deep learning enhances multiparametric dynamic volumetric photoacoustic computed tomography in vivo (DL-PACT). Adv. Sci., 10, 2202089(2023).

    [94] S. Jeon et al. A deep learning-based model that reduces speed of sound aberrations for improved in vivo photoacoustic imaging. IEEE Trans. Image Process., 30, 8773(2021).

    [95] Z. Cheng et al. 3D depth-coded photoacoustic microscopy with a large field of view for human skin imaging. Chin. Opt. Lett., 16, 081701(2018).

    [96] J. Ahn et al. Fully integrated photoacoustic microscopy and photoplethysmography of human in vivo. Photoacoustics, 27, 100374(2022).

    [97] Z. Wang et al. Photoacoustic and ultrasound (PAUS) dermoscope with high sensitivity and penetration depth by using a bimorph transducer. J. Biophotonics, 13, e202000145(2020).

    [98] Y. Gao et al. 4D spectral-spatial computational photoacoustic dermoscopy. Photoacoustics, 34, 100572(2023).

    [99] Z. Cheng et al. In vivo volumetric monitoring of revascularization of traumatized skin using extended depth-of-field photoacoustic microscopy. Front. Optoelectron., 13, 307(2020).

    [100] H. Ma et al. Quantitative and anatomical imaging of dermal angiopathy by noninvasive photoacoustic microscopic biopsy. Biomed. Opt. Express, 12, 6300(2021).

    [101] B. Hindelang et al. Optoacoustic mesoscopy shows potential to increase accuracy of allergy patch testing. Contact Dermatitis, 83, 206(2020).

    [102] B. Hindelang et al. Quantification of skin sensitivity to ultraviolet radiation using ultrawideband optoacoustic mesoscopy. Br. J. Dermatol., 184, 352(2021).

    [103] T. Nau et al. Raster-scanning optoacoustic mesoscopy biomarkers for atopic dermatitis skin lesions. Photoacoustics, 31, 100513(2023).

    [104] Y. W. Yew et al. Investigation of morphological, vascular and biochemical changes in the skin of an atopic dermatitis (AD) patient in response to dupilumab using raster scanning optoacoustic mesoscopy (RSOM) and handheld confocal Raman spectroscopy (CRS). J. Dermatol. Sci., 95, 123(2019).

    [105] X. Li et al. Multispectral raster-scanning optoacoustic mesoscopy differentiate lesional from non-lesional atopic dermatitis skin using structural and functional imaging markers. Photoacoustics, 28, 100399(2022).

    [106] X. Li et al. Structural and functional imaging of psoriasis for severity assessment and quantitative monitoring of treatment response using high-resolution optoacoustic imaging. Photoacoustics, 38, 100611(2024).

    [107] H. He et al. Opening a window to skin biomarkers for diabetes stage with optoacoustic mesoscopy. Light Sci. Appl., 12, 231(2023).

    [108] H. He et al. Fast optoacoustic mesoscopy of microvascular endothelial dysfunction in cardiovascular risk and disease. bioRxiv(2021).

    [109] C. P. Denton, D. Khanna. Systemic sclerosis. Lancet, 390, 1685(2017).

    [110] M. Masthoff et al. Multispectral optoacoustic tomography of systemic sclerosis. J. Biophotonics, 11, e201800155(2018).

    [111] R. Rosenberry, M. D. Nelson. Reactive hyperemia: a review of methods, mechanisms, and considerations. Am. J. Physiol. Regul. Integr. Comp. Physiol., 318, R605(2020).

    [112] L. Monteiro Rodrigues, T. F. Granja, S. F. de Andrade. Optoacoustic imaging offers new insights into in vivo human skin vascular physiology. Life, 12, 1628(2022).

    [113] H. Zhang et al. Quantitatively assessing port-wine stains using a photoacoustic imaging method: a pilot study. J. Am. Acad. Dermatol., 85, 1613(2021).

    [114] H. Ma et al. Switchable optical and acoustic resolution photoacoustic dermoscope dedicated into in vivo biopsy-like of human skin. Appl. Phys. Lett., 116, 073703(2020).

    [115] H. Ma et al. Three dimensional confocal photoacoustic dermoscopy with an autofocusing sono-opto probe. J. Biophotonics, 15, e202100323(2022).

    [116] H. Ma et al. Fast linear confocal scanning photoacoustic dermoscopy for non-invasive assessment of chromatodermatosis. Appl. Phys. Lett., 113, 083704(2018).

    [117] H. Ma et al. Multiscale confocal photoacoustic dermoscopy to evaluate skin health. Quantum Imaging Med. Surg., 12, 2696(2022).

    [118] Z. Wang et al. Bifocal 532/1064 nm alternately illuminated photoacoustic microscopy for capturing deep vascular morphology in human skin. J. Eur. Acad. Dermatol. Venereol., 36, 51(2022).

    [119] Z. Wang et al. Quantitative classification of melasma with photoacoustic microscopy: a pilot study. J. Biomed. Opt., 29, S11504(2024).

    [120] H. He et al. Fast raster-scan optoacoustic mesoscopy enables assessment of human melanoma microvasculature in vivo. Nat. Commun., 13, 2803(2022).

    [121] A. Berezhnoi et al. Optical features of human skin revealed by optoacoustic mesoscopy in the visible and short-wave infrared regions. Opt. Lett., 44, 4119(2019).

    [122] A. Breathnach et al. Preoperative measurement of cutaneous melanoma and nevi thickness with photoacoustic imaging. J. Med. Imaging, 5, 1(2018).

    [123] M. Crisan et al. Ultrasonographic staging of cutaneous malignant tumors: an ultrasonographic depth index. Arch. Dermatol. Res., 305, 305(2013).

    [124] J. Kim et al. Multispectral ex vivo photoacoustic imaging of cutaneous melanoma for better selection of the excision margin. Br. J. Dermatol., 179, 780(2018).

    [125] B. Park et al. 3D wide-field multispectral photoacoustic imaging of human melanomas in vivo: a pilot study. J. Eur. Acad. Dermatol. Venereol., 35, 669(2021).

    [126] A. F. Kukk et al. Combined ultrasound and photoacoustic C-mode imaging system for skin lesion assessment. Sci. Rep., 13, 17947(2023).

    [127] A. F. Kukk et al. Non-invasive 3D imaging of human melanocytic lesions by combined ultrasound and photoacoustic tomography: a pilot study. Sci. Rep., 14, 2768(2024).

    [128] A. E. Attia et al. Non-invasive photoacoustic 3D imaging of non-melanoma skin cancers in Asian population, CF3B.7(2018).

    [129] S. Y. Chuah et al. Volumetric multispectral optoacoustic tomography for 3-dimensional reconstruction of skin tumors: a further evaluation with histopathologic correlation. J. Invest. Dermatol., 139, 481(2019).

    [130] G. Fredman et al. Skin tags imaged by reflectance confocal microscopy, optical coherence tomography and multispectral optoacoustic tomography at the bedside. Skin Res. Technol., 27, 324(2021).

    [131] T. Von Knorring et al. Differentiation between benign and malignant pigmented skin tumours using bedside diagnostic imaging technologies: a pilot study. Acta Derm. Venereol., 102, adv00634(2022).

    [132] J. Yao, L. V. Wang. Sensitivity of photoacoustic microscopy. Photoacoustics, 2, 87(2014).

    [133] W. Xia et al. Handheld real-time LED-based photoacoustic and ultrasound imaging system for accurate visualization of clinical metal needles and superficial vasculature to guide minimally invasive procedures. Sensors, 18, 1394(2018).

    Junho Ahn, Minseong Kim, Chulhong Kim, Wonseok Choi, "In vivo multi-scale clinical photoacoustic imaging for analysis of skin vasculature and pigmentation: a comparative review," Adv. Imaging 1, 032002 (2024)
    Download Citation