Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The emerging role of photoacoustic imaging in clinical oncology

Abstract

Clinical oncology can benefit substantially from imaging technologies that reveal physiological characteristics with multiscale observations. Complementing conventional imaging modalities, photoacoustic imaging (PAI) offers rapid imaging (for example, cross-sectional imaging in real time or whole-breast scanning in 10–15 s), scalably high levels of spatial resolution, safe operation and adaptable configurations. Most importantly, this novel imaging modality provides informative optical contrast that reveals details on anatomical, functional, molecular and histological features. In this Review, we describe the current state of development of PAI and the emerging roles of this technology in cancer screening, diagnosis and therapy. We comment on the performance of cutting-edge photoacoustic platforms, and discuss their clinical applications and utility in various clinical studies. Notably, the clinical translation of PAI is accelerating in the areas of macroscopic and mesoscopic imaging for patients with breast or skin cancers, as well as in microscopic imaging for histopathology. We also highlight the potential of future developments in technological capabilities and their clinical implications, which we anticipate will lead to PAI becoming a desirable and widely used imaging modality in oncological research and practice.

Key points

  • Photoacoustic imaging (PAI) has emerged as an appealing modality that can complement existing imaging techniques for cancer screening, diagnosis and treatment guidance.

  • The elegant fusion of light and sound provides PAI with several distinctive capabilities including scalable spatial resolution and imaging depth while maintaining a high imaging speed.

  • By selecting suitable optical wavelengths, PAI can image a wide variety of endogenous molecules or exogenous agents, revealing the anatomy, histology, function and molecular activity of biological systems in vivo.

  • Taking advantage of the high sensitivity to tumour-associated hypoxia and angiogenesis, PAI has the potential to enable early detection of cancers of the breast, skin and prostate.

  • The role of PAI in clinical oncology has been demonstrated by the first FDA approval of this technology for breast cancer diagnosis; other areas of potential clinical application include cancer detection, biopsy guidance and molecular imaging.

  • In addition to cancer screening and diagnosis, PAI has shown potential benefit for the assessment of responses to neoadjuvant chemotherapy, guiding surgical resection and monitoring drug delivery.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Representative configurations and images of photoacoustic imaging.
Fig. 2: Representative photoacoustic contrasts in biological tissues.
Fig. 3: Representative in vivo photoacoustic imaging for cancer detection.
Fig. 4: PAI for cancer diagnosis.
Fig. 5: Photoacoustic imaging for assessment and guidance of cancer treatment.
Fig. 6: Selection of the PAI configurations and contrasts according to clinical applications.

Similar content being viewed by others

References

  1. Lin, L. et al. High-speed three-dimensional photoacoustic computed tomography for preclinical research and clinical translation. Nat. Commun. 12, 882 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Favazza, C. P., Jassim, O., Cornelius, L. A. & Wang, L. H. V. In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus. J. Biomed. Opt. 16, 016015 (2011).

    PubMed  PubMed Central  Google Scholar 

  3. Diot, G. et al. Multispectral optoacoustic tomography (MSOT) of human breast cancer. Clin. Cancer Res. 23, 6912–6922 (2017).

    Article  CAS  PubMed  Google Scholar 

  4. Kothapalli, S. R. et al. Simultaneous transrectal ultrasound and photoacoustic human prostate imaging. Sci. Transl. Med. 11, eaav2169 (2019).

    Article  PubMed  CAS  Google Scholar 

  5. Lin, L. et al. Single-breath-hold photoacoustic computed tomography of the breast. Nat. Commun. 9, 2352 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Lin, L. & Wang, L. H. V. in Advances in Experimental Medicine and Biology Vol. 3233 Ch. 8 (eds Wei, X. & Gu, B.) 147–175 (Springer, 2021).

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

    Article  PubMed  PubMed Central  Google Scholar 

  8. Steinberg, I. et al. Photoacoustic clinical imaging. Photoacoustics 14, 77–98 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Upputuri, P. K. & Pramanik, M. Recent advances toward preclinical and clinical translation of photoacoustic tomography: a review. J. Biomed. Opt. 22, 041006 (2017).

    Article  Google Scholar 

  10. Wang, L. H. V. & Yao, J. J. A practical guide to photoacoustic tomography in the life sciences. Nat. Methods 13, 627–638 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Valluru, K. S., Wilson, K. E. & Willmann, J. K. Photoacoustic imaging in oncology: translational preclinical and early clinical experience. Radiology 280, 332–349 (2016).

    Article  PubMed  Google Scholar 

  12. Li, L. et al. Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution. Nat. Biomed. Eng. 1, 0071 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Gargiulo, S., Albanese, S. & Mancini, M. State-of-the-art preclinical photoacoustic imaging in oncology: recent advances in cancer theranostics. Contrast. Media. Mol. Imaging 2019, 5080267 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Dean-Ben, X. L. & Razansky, D. Optoacoustic imaging of the skin. Exp. Dermatol. 30, 1598–1609 (2021).

    Article  PubMed  Google Scholar 

  15. Regensburger, A. P., Wagner, A. L., Claussen, J., Waldner, M. J. & Knieling, F. Shedding light on pediatric diseases: multispectral optoacoustic tomography at the doorway to clinical applications. Mol. Cell. Pediatr. 7, 1–6 (2020).

    Article  Google Scholar 

  16. Ravina, K. et al. Prospects of photo- and thermoacoustic imaging in neurosurgery. Neurosurgery 87, 11–24 (2020).

    Article  PubMed  Google Scholar 

  17. Wang, Y. et al. Preclinical evaluation of photoacoustic imaging as a novel noninvasive approach to detect an orthopaedic implant infection. J. Am. Acad. Orthop. Surg. 25, S7–S12 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhang, J., Duan, F., Liu, Y. & Nie, L. High-resolution photoacoustic tomography for early-stage cancer detection and its clinical translation. Radiol. Imaging Cancer 2, e190030 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Valluru, K. S. & Willmann, J. K. Clinical photoacoustic imaging of cancer. Ultrasonography 35, 267–280 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Taruttis, A., van Dam, G. M. & Ntziachristos, V. Mesoscopic and macroscopic optoacoustic imaging of cancer. Cancer Res. 75, 1548–1559 (2015).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Xia, J., Yao, J. J. & Wang, L. V. Photoacoustic tomography: principles and advances. Prog. Electromagn. Res. 147, 1–22 (2014).

    Article  Google Scholar 

  23. Wang, L. H. V. & Hu, S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science 335, 1458–1462 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rao, A. P., Bokde, N. & Sinha, S. Photoacoustic imaging for management of breast cancer: a literature review and future perspectives. Appl. Sci. Basel 10, 767 (2020).

    Article  CAS  Google Scholar 

  25. Nyayapathi, N. & Xia, J. Photoacoustic imaging of breast cancer: a mini review of system design and image features. J. Biomed. Opt. 24, 121911 (2019).

    Article  PubMed Central  Google Scholar 

  26. Attia, A. B. E. et al. Noninvasive real-time characterization of non-melanoma skin cancers with handheld optoacoustic probes. Photoacoustics 7, 20–26 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Stoffels, I. et al. Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging. Sci. Transl. Med. 7, 317ra199 (2015).

    Article  PubMed  CAS  Google Scholar 

  29. Hai, P. et al. Label-free high-throughput photoacoustic tomography of suspected circulating melanoma tumor cells in patients in vivo. J. Biomed. Opt. 25, 1–17 (2020).

    Article  PubMed  Google Scholar 

  30. Wong, T. T. W. et al. Fast label-free multilayered histology-like imaging of human breast cancer by photoacoustic microscopy. Sci. Adv. 3, e1602168 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Food and Drug Administration. Premarket Approval: Imagio Breast Imaging System (FDA, 2021).

  32. Laser Institute of America. ANSI Z136.1–2007: American National Standard for Safe Use of Lasers (LIA, 2007).

  33. Yao, J. J. & Wang, L. H. V. Photoacoustic microscopy. Laser Photonics Rev. 7, 758–778 (2013).

    Article  Google Scholar 

  34. Xu, M. H. & Wang, L. H. V. Universal back-projection algorithm for photoacoustic computed tomography. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71, 016706 (2005).

    Article  PubMed  CAS  Google Scholar 

  35. Guo, H., Li, Y., Qi, W. Z. & Xi, L. Photoacoustic endoscopy: a progress review. J. Biophotonics. 13, e202000217 (2020).

    Article  PubMed  Google Scholar 

  36. Yao, J. J. & Wang, L. H. V. Photoacoustic tomography: fundamentals, advances and prospects. Contrast Media Mol. Imaging 6, 332–345 (2011).

    Article  CAS  PubMed  Google Scholar 

  37. Yao, J. et al. High-speed label-free functional photoacoustic microscopy of mouse brain in action. Nat. Methods 12, 407–410 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lan, B. et al. High-speed widefield photoacoustic microscopy of small-animal hemodynamics. Biomed. Opt. Express 9, 4689–4701 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lin, L. et al. High-speed photoacoustic microscopy of mouse cortical microhemodynamics. J. Biophotonics 10, 792–798 (2017).

    Article  CAS  PubMed  Google Scholar 

  40. Park, K. et al. Handheld photoacoustic microscopy probe. Sci. Rep. 7, 13359 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Lin, L. et al. Handheld optical-resolution photoacoustic microscopy. J. Biomed. Opt. 22, 41002 (2017).

    Article  PubMed  Google Scholar 

  42. Na, S. et al. Massively parallel functional photoacoustic computed tomography of the human brain. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-021-00735-8 (2021).

    Article  PubMed  Google Scholar 

  43. Weber, J., Beard, P. C. & Bohndiek, S. E. Contrast agents for molecular photoacoustic imaging. Nat. Methods 13, 639–650 (2016).

    Article  CAS  PubMed  Google Scholar 

  44. Upputuri, P. K. & Pramanik, M. Recent advances in photoacoustic contrast agents for in vivo imaging. Wires Nanomed. Nanobi. 12, e1618 (2020).

    Article  Google Scholar 

  45. Li, M. C., Tang, Y. Q. & Yao, J. J. Photoacoustic tomography of blood oxygenation: a mini review. Photoacoustics 10, 65–73 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Folkman, J. Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15–18 (2002).

    Article  CAS  PubMed  Google Scholar 

  47. Weidner, N., Semple, J. P., Welch, W. R. & Folkman, J. Tumor angiogenesis and metastasis–correlation in invasive breast-carcinoma. N. Engl. J. Med. 324, 1–8 (1991).

    Article  CAS  PubMed  Google Scholar 

  48. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011).

    Article  CAS  PubMed  Google Scholar 

  49. Shi, J. H. et al. High-resolution, high-contrast mid-infrared imaging of fresh biological samples with ultraviolet-localized photoacoustic microscopy. Nat. Photonics 13, 609–615 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang, H. F., Maslov, K., Stoica, G. & Wang, L. H. V. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat. Biotechnol. 24, 848–851 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. Yao, J. J. & Wang, L. H. V. Recent progress in photoacoustic molecular imaging. Curr. Opin. Chem. Biol. 45, 104–112 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Collins, J. A., Rudenski, A., Gibson, J., Howard, L. & O’Driscoll, R. Relating oxygen partial pressure, saturation and content: the haemoglobin-oxygen dissociation curve. Breathe 11, 195–201 (2015).

    Article  Google Scholar 

  53. Grosenick, D., Rinneberg, H., Cubeddu, R. & Taroni, P. Review of optical breast imaging and spectroscopy. J. Biomed. Opt. 21, 091311 (2016).

    Article  PubMed  Google Scholar 

  54. Shah, J. et al. Photoacoustic imaging and temperature measurement for photothermal cancer therapy. J. Biomed. Opt. 13, 034024 (2008).

    Article  PubMed  Google Scholar 

  55. Yao, J. J., Maslov, K. I., Zhang, Y., Xia, Y. N. & Wang, L. V. Label-free oxygen-metabolic photoacoustic microscopy in vivo. J. Biomed. Opt. 16, 076003 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Jiang, Y. & Zemp, R. Estimation of cerebral metabolic rate of oxygen consumption using combined multiwavelength photoacoustic microscopy and Doppler microultrasound. J. Biomed. Opt. 23, 016009 (2018).

    Google Scholar 

  57. Singh, P. et al. Gold nanoparticles in diagnostics and therapeutics for human cancer. Int. J. Mol. Sci. 19, 1979 (2018).

    Article  PubMed Central  CAS  Google Scholar 

  58. Li, W. W. & Chen, X. Y. Gold nanoparticles for photoacoustic imaging. Nanomedicine 10, 299–320 (2015).

    Article  CAS  PubMed  Google Scholar 

  59. Okumura, K. et al. Photoacoustic imaging of tumour vascular permeability with indocyanine green in a mouse model. Eur. Radiol. Exp. 2, 5 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Garcia-Uribe, A. et al. Dual-modality photoacoustic and ultrasound imaging system for noninvasive sentinel lymph node detection in patients with breast cancer. Sci. Rep. 5, 15748 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Forbrich, A., Heinmiller, A. & Zemp, R. J. Photoacoustic imaging of lymphatic pumping. J. Biomed. Opt. 22, 1–6 (2017).

    Article  PubMed  Google Scholar 

  62. Toi, M. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Dumani, D. S. et al. in Proceedings of SPIE. Vol. 10494: Photons Plus Ultrasound: Imaging and Sensing 2018 (eds Oraevsky, A. A. & Wang, L. V.) 10494 2W (SPIE, 2018).

  64. Hosseinaee, Z., Simmons, J. A. T. & Reza, P. H. Dual-modal photoacoustic imaging and optical coherence tomography [review]. Front. Phys. 8, 635 (2021).

    Article  Google Scholar 

  65. Park, J. et al. Quadruple ultrasound, photoacoustic, optical coherence, and fluorescence fusion imaging with a transparent ultrasound transducer. Proc. Natl Acad. Sci. USA 118, e1920879118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Song, W. et al. Fully integrated reflection-mode photoacoustic, two-photon, and second harmonic generation microscopy in vivo. Sci. Rep. 6, 32240 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Rao, B., Soto, F., Kerschensteiner, D. & Wang, L. H. V. Integrated photoacoustic, confocal, and two-photon microscope. J. Biomed. Opt. 19, 36002 (2014).

    Article  PubMed  CAS  Google Scholar 

  68. Fass, L. Imaging and cancer: a review. Mol. Oncol. 2, 115–152 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ariztia, E. V., Lee, C. J., Gogoi, R. & Fishman, D. A. The tumor microenvironment: key to early detection. Crit. Rev. Clin. Lab. Sci. 43, 393–425 (2006).

    Article  CAS  PubMed  Google Scholar 

  70. Muz, B., de la Puente, P., Azab, F. & Azab, A. K. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia 3, 83–92 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Hockel, M. & Vaupel, P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl Cancer Inst. 93, 266–276 (2001).

    Article  CAS  PubMed  Google Scholar 

  72. von Euler-Chelpin, M., Lillholm, M., Vejborg, I., Nielsen, M. & Lynge, E. Sensitivity of screening mammography by density and texture: a cohort study from a population-based screening program in Denmark. Breast Cancer Res. 21, 111 (2019).

    Article  CAS  Google Scholar 

  73. Devolli-Disha, E., Manxhuka-Kerliu, S., Ymeri, H. & Kutllovci, A. Comparative accuracy of mammography and ultrasound in women with breast symptoms according to age and breast density. Bosn. J. Basic. Med. 9, 131–136 (2009).

    Article  Google Scholar 

  74. Moss, S., Faulkner, K., Law, J. & Young, K. Benefits versus risks from mammography–a critical reassessment. Cancer 79, 628–628 (1997).

    Article  CAS  PubMed  Google Scholar 

  75. Sim, L. S. J., Hendriks, J. H. C. L. & Fook-Chong, S. M. C. Breast ultrasound in women with familial risk of breast cancer. Ann. Acad. Med. Singap. 33, 600–606 (2004).

    CAS  PubMed  Google Scholar 

  76. Boudreau, N. & Myers, C. Breast cancer-induced angiogenesis: multiple mechanisms and the role of the microenvironment. Breast Cancer Res. 5, 140–146 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27–31 (1995).

    Article  CAS  PubMed  Google Scholar 

  78. Banerjee, S., Dowsett, M., Ashworth, A. & Martin, L. A. Mechanisms of disease: angiogenesis and the management of breast cancer. Nat. Clin. Pract. Oncol. 4, 536–550 (2007).

    Article  CAS  PubMed  Google Scholar 

  79. Pavlakis, K. et al. The assessment of angiogenesis and fibroblastic stromagenesis in hyperplastic and pre-invasive breast lesions. BMC Cancer 8, 88 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Vogl, G., Dietze, O. & Hauser-Kronberger, C. Angiogenic potential of ductal carcinoma in situ (DCIS) of human breast. Histopathology 47, 617–624 (2005).

    Article  CAS  PubMed  Google Scholar 

  81. Viacava, P. et al. Angiogenesis and VEGF expression in pre-invasive lesions of the human breast. J. Pathol. 204, 140–146 (2004).

    Article  CAS  PubMed  Google Scholar 

  82. Cao, Y., Paner, G. P., Kahn, L. B. & Rajan, P. B. Noninvasive carcinoma of the breast–angiogenesis and cell proliferation. Arch. Pathol. Lab. Med. 128, 893–896 (2004).

    Article  PubMed  Google Scholar 

  83. Teo, N. B. et al. Vascular density and phenotype around ductal carcinoma in situ (DCIS) of the breast. Br. J. Cancer 86, 905–911 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Heffelfinger, S. C., Miller, M. A., Yassin, R. & Gear, R. Angiogenic growth factors in preinvasive breast disease. Clin. Cancer Res. 5, 2867–2876 (1999).

    CAS  PubMed  Google Scholar 

  85. Heffelfinger, S. C., Yassin, R., Miller, M. A. & Lower, E. Vascularity of proliferative breast disease and carcinoma in situ correlates with histological features. Clin. Cancer Res. 2, 1873–1878 (1996).

    CAS  PubMed  Google Scholar 

  86. Carpenter, P. M., Chen, W. P., Mendez, A., McLaren, C. E. & Su, M. Y. Angiogenesis in the progression of breast ductal proliferations. Int. J. Surg. Pathol. 19, 335–341 (2011).

    Article  PubMed  Google Scholar 

  87. Bluff, J. E. et al. Angiogenesis is associated with the onset of hyperplasia in human ductal breast disease. Br. J. Cancer 101, 666–672 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Nagy, J. A., Chang, S. H., Dvorak, A. M. & Dvorak, H. F. Why are tumour blood vessels abnormal and why is it important to know? Br. J. Cancer 100, 865–869 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Gordon, M. S., Mendelson, D. S. & Kato, G. Tumor angiogenesis and novel antiangiogenic strategies. Int. J. Cancer 126, 1777–1787 (2010).

    Article  CAS  PubMed  Google Scholar 

  90. Madu, C. O., Wang, S., Madu, C. O. & Lu, Y. Angiogenesis in breast cancer progression, diagnosis, and treatment. J. Cancer 11, 4474–4494 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Manohar, S. & Dantuma, M. Current and future trends in photoacoustic breast imaging. Photoacoustics 16, 100134 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Zhang, G. J., Li, W. Z., Yang, M. & Li, C. H. Developing a photoacoustic whole-breast imaging system based on the synthetic matrix array. Front. Phys. https://doi.org/10.3389/fphy.2020.600589 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Nyayapathi, N. et al. Dual scan mammoscope (DSM)–a new portable photoacoustic breast imaging system with scanning in craniocaudal plane. IEEE Trans. Biomed. Eng. 67, 1321–1327 (2020).

    Article  PubMed  Google Scholar 

  94. Heijblom, M. et al. The state of the art in breast imaging using the Twente photoacoustic mammoscope: results from 31 measurements on malignancies. Eur. Radiol. 26, 3874–3887 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Schoustra, S. M. et al. Twente photoacoustic mammoscope 2: system overview and three-dimensional vascular network images in healthy breasts. J. Biomed. Opt. 24, 1–12 (2019).

    Article  PubMed  Google Scholar 

  96. Oraevsky, A. et al. in Proceedings of SPIE. Vol. 10494: Photons Plus Ultrasound: Imaging and Sensing 2018 (eds Oraevsky, A. A. & Wang, L. V.) 10494 2Y (SPIE, 2018).

  97. Matsumoto, Y. et al. Visualising peripheral arterioles and venules through high-resolution and large-area photoacoustic imaging. Sci. Rep. 8, 14930 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Hu, P., Li, L., Lin, L. & Wang, L. H. V. Spatiotemporal antialiasing in photoacoustic computed tomography. IEEE Trans. Med. Imaging 39, 3535–3547 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Bohndiek, S. Addressing photoacoustics standards. Nat. Photonics 13, 298–298 (2019).

    Article  CAS  Google Scholar 

  100. Kaplan, S. S. Automated whole breast ultrasound. Radiol. Clin. North Am. 52, 539–546 (2014).

    Article  PubMed  Google Scholar 

  101. Leong, L. C., Gogna, A., Pant, R., Ng, F. C. & Sim, L. S. Supplementary breast ultrasound screening in Asian women with negative but dense mammograms–a pilot study. Ann. Acad. Med. Singap. 41, 432–439 (2012).

    PubMed  Google Scholar 

  102. Rhodes, A. R. Public-education and cancer of the skin-What do people need to know about melanoma and nonmelanoma skin-cancer. Cancer 75, 613–636 (1995).

    Article  CAS  PubMed  Google Scholar 

  103. Lutz, K., Hayward, V., Joseph, M., Wong, E. & Temple-Oberle, C. Current biopsy practices for suspected melanoma: a survey of family physicians in Southwestern Ontario. Plast. Surg. 22, 175–178 (2014).

    Article  Google Scholar 

  104. Dummer, W. et al. Preoperative characterization of pigmented skin lesions by epiluminescence microscopy and high-frequency ultrasound. Arch. Dermatol. 131, 279–285 (1995).

    Article  CAS  PubMed  Google Scholar 

  105. Hult, J. et al. Comparison of photoacoustic imaging and histopathological examination in determining the dimensions of 52 human melanomas and nevi ex vivo. Biomed. Opt. Express 12, 4097–4114 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  106. von Knorring, T. & Mogensen, M. Photoacoustic tomography for assessment and quantification of cutaneous and metastatic malignant melanoma–a systematic review. Photodiagnosis Photodyn. Ther. 33, 102095 (2021).

    Article  Google Scholar 

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

    Article  Google Scholar 

  108. Nagae, K. et al. Real-time 3D photoacoustic visualization system with a wide field of view for imaging human limbs. F1000Res 7, 1813 (2018).

    Article  PubMed  Google Scholar 

  109. Brown, E., Brunker, J. & Bohndiek, S. E. Photoacoustic imaging as a tool to probe the tumour microenvironment. Dis. Model Mech. https://doi.org/10.1242/dmm.039636 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Breathnach, A. et al. Preoperative measurement of cutaneous melanoma and nevi thickness with photoacoustic imaging. J. Med. Imaging 5, 015004 (2018).

    Article  Google Scholar 

  111. 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).

    Article  PubMed  Google Scholar 

  112. Jathoul, A. P. et al. Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinase-based genetic reporter. Nat. Photonics 9, 239–246 (2015).

    Article  CAS  Google Scholar 

  113. Chen, Z. et al. Non-invasive multimodal optical coherence and photoacoustic tomography for human skin imaging. Sci. Rep. 7, 17975 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Catalona, W. J., Smith, D. S., Ratliff, T. L. & Basler, J. W. Detection of organ-confined prostate-cancer is increased through prostate-specific antigen-based screening. JAMA 270, 948–954 (1993).

    Article  CAS  PubMed  Google Scholar 

  115. 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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Li, Y., Lu, G. X., Zhou, Q. F. & Chen, Z. P. Advances in endoscopic photoacoustic imaging. Photonics 8, 281 (2021).

    Article  CAS  PubMed  Google Scholar 

  117. Basij, M. et al. Miniaturized phased-array ultrasound and photoacoustic endoscopic imaging system. Photoacoustics 15, 100139 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Dangi, A. et al. in Proceedings of SPIE. Vol. 10878: Photons Plus Ultrasound: Imaging and Sensing 2019 (eds Oraevsky, A. A. & Wang, L. V.) (SPIE, 2019).

  119. Yang, G. et al. Co-registered photoacoustic and ultrasound imaging of human colorectal cancer. J. Biomed. Opt. 24, 1–13 (2019).

    PubMed  Google Scholar 

  120. Yang, J. M. et al. Three-dimensional photoacoustic endoscopic imaging of the rabbit esophagus. PloS ONE 10, e0120269 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Yang, M. et al. Photoacoustic/ultrasound dual imaging of human thyroid cancers: an initial clinical study. Biomed. Opt. Express 8, 3449–3457 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Salehi, H. S. et al. Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies. J. Biomed. Opt. 21, 46006 (2016).

    Article  PubMed  Google Scholar 

  123. Nandy, S. et al. Evaluation of ovarian cancer: initial application of coregistered photoacoustic tomography and US. Radiology 289, 740–747 (2018).

    Article  PubMed  Google Scholar 

  124. Yan, Y. et al. Spectroscopic photoacoustic imaging of cervical tissue composition in excised human samples. PloS ONE 16, e0247385 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Dogra, V. S. et al. Preliminary results of ex vivo multispectral photoacoustic imaging in the management of thyroid cancer. Am. J. Roentgenol. 202, W552–W558 (2014).

    Article  Google Scholar 

  126. Mitrayana, Apriyanto, D. K. & Satriawan, M. CO2 laser photoacoustic spectrometer for measuring acetone in the breath of lung cancer patients. Biosensors 10, 55 (2020).

    Article  CAS  PubMed Central  Google Scholar 

  127. Butler, R. et al. Optoacoustic breast imaging: imaging-pathology correlation of optoacoustic features in benign and malignant breast masses. Am. J. Roentgenol. 211, 1155–1170 (2018).

    Article  Google Scholar 

  128. de Heer, E. C., Jalving, M. & Harris, A. L. HIFs, angiogenesis, and metabolism: elusive enemies in breast cancer. J. Clin. Invest. 130, 5074–5087 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Oraevsky, A. A. et al. Clinical optoacoustic imaging combined with ultrasound for coregistered functional and anatomical mapping of breast tumors. Photoacoustics 12, 30–45 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Neuschler, E. I. et al. A pivotal study of optoacoustic imaging to diagnose benign and malignant breast masses: a new evaluation tool for radiologists. Radiology 287, 398–412 (2018).

    Article  PubMed  Google Scholar 

  131. Menezes, G. L. G. et al. Downgrading of breast masses suspicious for cancer by using optoacoustic breast imaging. Radiology 288, 355–365 (2018).

    Article  PubMed  Google Scholar 

  132. Dogan, B. E. et al. Optoacoustic imaging and gray-scale US features of breast cancers: correlation with molecular subtypes. Radiology 292, 564–572 (2019).

    Article  PubMed  Google Scholar 

  133. Food and Drug Administration. Summary of safety and effectiveness data (SSED): Imagio® breast imaging system. https://www.accessdata.fda.gov/cdrh_docs/pdf20/P200003B.pdf (2021).

  134. Xu, Y., Wang, L. V., Ambartsoumian, G. & Kuchment, P. Reconstructions in limited-view thermoacoustic tomography. Med. Phys. 31, 724–733 (2004).

    Article  PubMed  Google Scholar 

  135. Li, G. et al. Tripling the detection view of high-frequency linear-array-based photoacoustic computed tomography by using two planar acoustic reflectors. Quant. Imaging Med. Surg. 5, 57–62 (2015).

    PubMed  PubMed Central  Google Scholar 

  136. Zhang, R. et al. Exploring the diagnostic value of photoacoustic imaging for breast cancer: the identification of regional photoacoustic signal differences of breast tumors. Biomed. Opt. Express 12, 1407–1421 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Zalev, J. et al. Opto-acoustic imaging of relative blood oxygen saturation and total hemoglobin for breast cancer diagnosis. J. Biomed. Opt. 24, 121915 (2019).

    Article  PubMed Central  Google Scholar 

  138. Fakhrejahani, E. et al. Clinical report on the first prototype of a photoacoustic tomography system with dual illumination for breast cancer imaging. PloS ONE 10, e0139113 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Yang, M. et al. Quantitative analysis of breast tumours aided by three-dimensional photoacoustic/ultrasound functional imaging. Sci. Rep. 10, 8047 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Neal, L. et al. Diagnosis and management of benign, atypical, and indeterminate breast lesions detected on core needle biopsy. Mayo Clin. Proc. 89, 536–547 (2014).

    Article  PubMed  Google Scholar 

  141. Faries, M. B. et al. Lymph node metastasis in melanoma: a debate on the significance of nodal metastases, conditional survival analysis and clinical trials. Clin. Exp. Metastas-. 35, 431–442 (2018).

    Article  Google Scholar 

  142. He, Y. et al. In vivo label-free photoacoustic flow cytography and on-the-spot laser killing of single circulating melanoma cells. Sci. Rep. 6, 39616 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Vogl, T. & Bisdas, S. Lymph node staging. Top. Magn. Reson. Imaging 18, 303–316 (2007).

    Article  PubMed  Google Scholar 

  144. Hsueh, E. C., Hansen, N. & Giuliano, A. E. Intraoperative lymphatic mapping and sentinel lymph node dissection in breast cancer. Cancer J. Clin. 50, 279–291 (2000).

    Article  CAS  Google Scholar 

  145. Liu, S. D. et al. In vivo photoacoustic sentinel lymph node imaging using clinically-approved carbon nanoparticles. IEEE Trans. Biomed. Eng. 67, 2033–2042 (2020).

    PubMed  Google Scholar 

  146. Kim, C. et al. Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes. J. Biomed. Opt. 15, 046010 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Kang, J. et al. Real-time sentinel lymph node biopsy guidance using combined ultrasound, photoacoustic, fluorescence imaging: in vivo proof-of-principle and validation with nodal obstruction. Sci. Rep. 7, 45008 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Wang, H. et al. Three-dimensional interventional photoacoustic imaging for biopsy needle guidance with a linear array transducer. J. Biophotonics 12, e201900212 (2019).

    Article  CAS  PubMed  Google Scholar 

  149. Piras, D., Grijsen, C., Schutte, P., Steenbergen, W. & Manohar, S. Photoacoustic needle: minimally invasive guidance to biopsy. J. Biomed. Opt. 18, 070502 (2013).

    Article  PubMed  Google Scholar 

  150. Chen, Z. Y. et al. Advance of molecular imaging technology and targeted imaging agent in imaging and therapy. Biomed. Res. Int. 2014, 19324 (2014).

    Google Scholar 

  151. National Center for Biotechnology Information. Molecular imaging and contrast agent database (MICAD) (National Center for Biotechnology Information, 2004–2013).

  152. Tummers, W. S. et al. Intraoperative pancreatic cancer detection using tumor-specific multimodality molecular imaging. Ann. Surg. Oncol. 25, 1880–1888 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  153. Sano, K. et al. In vivo photoacoustic imaging of cancer using indocyanine green-labeled monoclonal antibody targeting the epidermal growth factor receptor. Biochem. Biophys. Res. Commun. 464, 820–825 (2015).

    Article  CAS  PubMed  Google Scholar 

  154. Giusti, R. M., Shastri, K. A., Cohen, M. H., Keegan, P. & Pazdur, R. FDA drug approval summary: Panitumumab (Vectibix). Oncologist 12, 577–583 (2007).

    Article  CAS  PubMed  Google Scholar 

  155. Cong, F., Yu, H. & Gao, X. Expression of CD24 and B7-H3 in breast cancer and the clinical significance. Oncol. Lett. 14, 7185–7190 (2017).

    PubMed  PubMed Central  Google Scholar 

  156. Wilson, K. E. et al. Spectroscopic photoacoustic molecular imaging of breast cancer using a B7-H3-targeted ICG contrast agent. Theranostics 7, 1463–1476 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Korde, L. A. et al. Neoadjuvant chemotherapy, endocrine therapy, and targeted therapy for breast cancer: ASCO guideline. J. Clin. Oncol. 39, 1485–1505 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Davidson, N. E. & Morrow, M. Sometimes a great notion–an assessment of neoadjuvant systemic therapy for breast cancer. J. Natl Cancer I 97, 159–161 (2005).

    Article  Google Scholar 

  159. Cortazar, P. & Kluetz, P. G. Neoadjuvant breast cancer therapy and drug development. Clin. Adv. Hematol. Oncol. 13, 755–761 (2015).

    PubMed  Google Scholar 

  160. Cocconi, G. et al. Problems in evaluating response of primary breast-cancer to systemic therapy. Breast Cancer Res. Treat. 4, 309–313 (1984).

    Article  CAS  PubMed  Google Scholar 

  161. Lin, L. et al. Photoacoustic computed tomography of breast cancer in response to neoadjuvant chemotherapy. Adv. Sci. 8, 2003396 (2021).

    Article  CAS  Google Scholar 

  162. Li, X. et al. Functional photoacoustic tomography of breast cancer: pilot clinical results. Biomed. Opt. https://doi.org/10.1364/BIOMED.2014.BS3A.63 (2014).

    Article  Google Scholar 

  163. Wiacek, A. & Bell, M. A. L. Photoacoustic-guided surgery from head to toe [invited]. Biomed. Opt. Express 12, 2079–2117 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  164. Moran, M. S. et al. Society of Surgical Oncology–American Society for Radiation Oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in stages I and II invasive breast cancer. J. Clin. Oncol. 32, 1507–1515 (2014).

    Article  PubMed  Google Scholar 

  165. Yao, D. K., Maslov, K., Shung, K. K., Zhou, Q. F. & Wang, L. V. In vivo label-free photoacoustic microscopy of cell nuclei by excitation of DNA and RNA. Opt. Lett. 35, 4139–4141 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Imai, T. et al. High-throughput ultraviolet photoacoustic microscopy with multifocal excitation. J. Biomed. Opt. 23, 1–6 (2018).

    Article  PubMed  Google Scholar 

  167. Kim, G. R. et al. Photoacoustic imaging of breast microcalcifications: a preliminary study with 8-gauge core-biopsied breast specimens. PloS ONE 9, e105878 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Asgari, S., Röhrborn, H.-J., Engelhorn, T., Fauser, B. & Stolke, D. Intraoperative measurement of cortical oxygen saturation and blood volume adjacent to cerebral arteriovenous malformations using near-infrared spectroscopy. Neurosurgery 52, 1298–1306 (2003).

    Article  PubMed  Google Scholar 

  169. Moradi, H., Tang, S. & Salcudean, S. E. Toward robot-assisted photoacoustic imaging: implementation using the da Vinci research kit and virtual fixtures. IEEE Robot. Autom. Let. 4, 1807–1814 (2019).

    Article  Google Scholar 

  170. Gandhi, N., Allard, M., Kim, S., Kazanzides, P. & Bell, M. A. L. Photoacoustic-based approach to surgical guidance performed with and without a da Vinci robot. J. Biomed. Opt. 22, 121606 (2017).

    Article  PubMed Central  Google Scholar 

  171. Gilmour, D. T., Das, S. & Flowerdew, G. Rates of urinary tract injury from gynecologic surgery and the role of intraoperative cystoscopy. Obstet. Gynecol. 107, 1366–1372 (2006).

    Article  CAS  PubMed  Google Scholar 

  172. Delacroix, S. E. & Winters, J. Urinary tract injures: recognition and management. Clin. Colon. Rectal Surg. 23, 104–112 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  173. Allard, M., Shubert, J. & Bell, M. A. L. Feasibility of photoacoustic-guided teleoperated hysterectomies. J. Med. Imaging 5, 021213 (2018).

    Article  Google Scholar 

  174. Bell, M. A. L., Ostrowski, A. K., Li, K., Kazanzides, P. & Boctor, E. M. Localization of transcranial targets for photoacoustic-guided endonasal surgeries. Photoacoustics 3, 78–87 (2015).

    Article  Google Scholar 

  175. Graham, M. T., Huang, J. Q., Creighton, F. X. & Bell, M. A. L. Simulations and human cadaver head studies to identify optimal acoustic receiver locations for minimally invasive photoacoustic-guided neurosurgery. Photoacoustics 19, 100183 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Moore, C. & Jokerst, J. V. Strategies for image-guided therapy, surgery, and drug delivery using photoacoustic imaging. Theranostics 9, 1550–1571 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Kircher, M. F. et al. A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle. Nat. Med. 18, 829–834 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Grootendorst, D. J. et al. Evaluation of superparamagnetic iron oxide nanoparticles (Endorem (R)) as a photoacoustic contrast agent for intra-operative nodal staging. Contrast Media Mol. Imaging 8, 83–91 (2013).

    Article  CAS  PubMed  Google Scholar 

  179. Xi, L. et al. Photoacoustic and fluorescence image-guided surgery using a multifunctional targeted nanoprobe. Ann. Surg. Oncol. 21, 1602–1609 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  180. Zhang, Y. Q., Yu, J. C., Kahkoska, A. R. & Gu, Z. Photoacoustic drug delivery. Sensors 17, 1400 (2017).

    Article  CAS  PubMed Central  Google Scholar 

  181. Wu, Z. G. et al. A microrobotic system guided by photoacoustic computed tomography for targeted navigation in intestines in vivo. Sci. Robot 4, eaax0613 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  182. Huang, X. H., El-Sayed, I. H., Qian, W. & El-Sayed, M. A. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Chem. Soc. 128, 2115–2120 (2006).

    Article  CAS  PubMed  Google Scholar 

  183. Nie, L. M. et al. In vivo volumetric photoacoustic molecular angiography and therapeutic monitoring with targeted plasmonic nanostars. Small 10, 1585–1593 (2014).

    Article  CAS  PubMed  Google Scholar 

  184. Moon, G. D. et al. A new theranostic system based on gold nanocages and phase-change materials with unique features for photoacoustic imaging and controlled release. J. Am. Chem. Soc. 133, 4762–4765 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Manivasagan, P. et al. Doxorubicin-loaded fucoidan capped gold nanoparticles for drug delivery and photoacoustic imaging. Int. J. Biol. Macromol. 91, 578–588 (2016).

    Article  CAS  PubMed  Google Scholar 

  186. Zhong, J. P., Yang, S. H., Wen, L. W. & Xing, D. Imaging-guided photoacoustic drug release and synergistic chemo-photoacoustic therapy with paclitaxel-containing nanoparticles. J. Control. Rel. 226, 77–87 (2016).

    Article  CAS  Google Scholar 

  187. Lovell, J. F. et al. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat. Mater. 10, 324–332 (2011).

    Article  CAS  PubMed  Google Scholar 

  188. Hannah, A., Luke, G., Wilson, K., Homan, K. & Emelianov, S. Indocyanine green-loaded photoacoustic nanodroplets: dual contrast nanoconstructs for enhanced photoacoustic and ultrasound imaging. Acs Nano 8, 250–259 (2014).

    Article  CAS  PubMed  Google Scholar 

  189. Li, X. S., Lovell, J. F., Yoon, J. & Chen, X. Y. Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. 17, 657–674 (2020).

    Article  PubMed  Google Scholar 

  190. Liu, Y. J., Bhattarai, P., Dai, Z. F. & Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 48, 2053–2108 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. De La Zerda, A. et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat. Nanotechnol. 3, 557–562 (2008).

    Article  PubMed  CAS  Google Scholar 

  192. Shashkov, E. V., Everts, M., Galanzha, E. I. & Zharov, V. P. Quantum dots as multimodal photoacoustic and photothermal contrast agents. Nano Lett. 8, 3953–3958 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Rastinehad, A. R. et al. Gold nanoshell-localized photothermal ablation of prostate tumors in a clinical pilot device study. Proc. Natl Acad. Sci. USA 116, 18590–18596 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Sharman, W. M., Allen, C. M. & van Lier, J. E. Photodynamic therapeutics: basic principles and clinical applications. Drug Discov. Today 4, 507–517 (1999).

    Article  CAS  PubMed  Google Scholar 

  195. Wan, M. T. & Lin, J. Y. Current evidence and applications of photodynamic therapy in dermatology. Clin. Cosmet. Invest. Dermatol. 7, 145 (2014).

    Google Scholar 

  196. Qumseya, B. J., David, W. & Wolfsen, H. C. Photodynamic therapy for Barrett’s esophagus and esophageal carcinoma. Clin. Endosc. 46, 30 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  197. Simone, C. B.II & Cengel, K. A. Photodynamic therapy for lung cancer and malignant pleural mesothelioma. Semin. Oncol. 41, 820–830 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Gheewala, T., Skwor, T. & Munirathinam, G. Photosensitizers in prostate cancer therapy. Oncotarget 8, 30524 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  199. Ho, C. J. H. et al. Multifunctional photosensitizer-based contrast agents for photoacoustic imaging. Sci. Rep. 4, 5342 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Srivatsan, A. et al. Gold nanocage-photosensitizer conjugates for dual-modal image-guided enhanced photodynamic therapy. Theranostics 4, 163–174 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  201. Lin, J. et al. Photosensitizer-loaded gold vesicles with strong plasmonic coupling effect for imaging-guided photothermal/photodynamic therapy. ACS Nano 7, 5320–5329 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Liu, T. et al. Combined photothermal and photodynamic therapy delivered by PEGylated MoS2 nanosheets. Nanoscale 6, 11219–11225 (2014).

    Article  CAS  PubMed  Google Scholar 

  203. Guo, W. et al. Multifunctional theranostic agent of Cu2(OH)PO4 quantum dots for photoacoustic image-guided photothermal/photodynamic combination cancer therapy. ACS Appl. Mater. Interfaces 9, 9348–9358 (2017).

    Article  CAS  PubMed  Google Scholar 

  204. Bell, M. A. L., Kuo, N. P., Song, D. Y., Kang, J. U. & Boctor, E. M. In vivo visualization of prostate brachytherapy seeds with photoacoustic imaging. J. Biomed. Opt. 19, 126011 (2014).

    Article  Google Scholar 

  205. Kuo, N., Kang, H. J., Song, D. Y., Kang, J. U. & Boctor, E. M. Real-time photoacoustic imaging of prostate brachytherapy seeds using a clinical ultrasound system. J. Biomed. Opt. 17, 066005 (2012).

    Article  PubMed  Google Scholar 

  206. Su, J. L., Bouchard, R. R., Karpiouk, A. B., Hazle, J. D. & Emelianov, S. Y. Photoacoustic imaging of prostate brachytherapy seeds. Biomed. Opt. Express 2, 2243–2254 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  207. Das, D., Sharma, A., Rajendran, P. & Pramanik, M. Another decade of photoacoustic imaging. Phys. Med. Biol. https://doi.org/10.1088/1361-6560/abd669 (2021).

    Article  PubMed  Google Scholar 

  208. Yang, W. H., Xu, J., Mu, J. B. & Xie, J. Revision of the concept of anti-angiogenesis and its applications in tumor treatment. Chronic Dis. Transl. Med. 3, 33–40 (2017).

    PubMed  PubMed Central  Google Scholar 

  209. Pinker, K. et al. Clinical application of bilateral high temporal and spatial resolution dynamic contrast-enhanced magnetic resonance imaging of the breast at 7 T. Eur. Radiol. 24, 913–920 (2014).

    Article  CAS  PubMed  Google Scholar 

  210. Nael, K. et al. High-spatial-resolution contrast-enhanced MR angiography of abdominal arteries with parallel acquisition at 3.0 T: initial experience in 32 patients. Am. J. Roentgenol. 187, W77–W85 (2006).

    Article  Google Scholar 

  211. Zhuang, B. et al. in Proc. 2012. IEEE Int. Ultrasonics Symp 1662–1665 (IEEE, 2012).

  212. Pagliari, C. M. et al. Diagnostic quality of 50 and 100 µm computed radiography compared with screen-film mammography in operative breast specimens. Br. J. Radiol. 85, 910–916 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Rangayyan, R. M., Nguyen, T. M., Ayres, F. J. & Nandi, A. K. Effect of pixel resolution on texture features of breast masses in mammograms. J. Digit. Imaging 23, 547–553 (2010).

    Article  PubMed  Google Scholar 

  214. Prieto, E. et al. Evaluation of spatial resolution of a PET scanner through the simulation and experimental measurement of the recovery coefficient. Comput. Biol. Med. 40, 75–80 (2010).

    Article  CAS  PubMed  Google Scholar 

  215. Weinstein, S. P., Conant, E. F. & Sehgal, C. Technical advances in breast ultrasound imaging. Semin. Ultrasound CT MR 27, 273–283 (2006).

    Article  PubMed  Google Scholar 

  216. Kanal, K. M. et al. ACR–AAPM–SIIM practice guideline for determinants of image quality in digital mammography. J. Digit. Imaging 26, 10–25 (2013).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  218. Harvey, S. C. et al. An abbreviated protocol for high-risk screening breast MRI saves time and resources. J. Am. Coll. Radiol. 13, 374–380 (2016).

    Article  PubMed  Google Scholar 

  219. Dogan, B. E. et al. American College of Radiology-compliant short protocol breast MRI for high-risk breast cancer screening: a prospective feasibility study. Am. J. Roentgenol. 210, 214–221 (2018).

    Article  Google Scholar 

  220. Huppe, A. I. et al. Automated breast ultrasound interpretation times: a reader performance study. Acad. Radiol. 25, 1577–1581 (2018).

    Article  PubMed  Google Scholar 

  221. Bernardi, D. et al. Application of breast tomosynthesis in screening: incremental effect on mammography acquisition and reading time. Br. J. Radiol. 85, E1174–E1178 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Hernandez, T. G. et al. Performance evaluation of a high resolution dedicated breast PET scanner. Med. Phys. 43, 2261 (2016).

    Article  Google Scholar 

  223. Fowler, A. M. et al. Measuring glucose uptake in primary invasive breast cancer using simultaneous time-of-flight breast PET/MRI: a method comparison study with prone PET/CT. Radiol. Imaging Cancer 3, e200091 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  224. Zhao, T., Desjardins, A. E., Ourselin, S., Vercauteren, T. & Xia, W. Minimally invasive photoacoustic imaging: current status and future perspectives. Photoacoustics 16, 100146 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  225. Manohar, S. & Razansky, D. Photoacoustics: a historical review. Adv. Opt. Photonics 8, 586–617 (2016).

    Article  Google Scholar 

  226. Guo, Z. J., Li, L. & Wang, L. H. V. On the speckle-free nature of photoacoustic tomography. Med. Phys. 36, 4084–4088 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  227. Lin, J. C. Microwave thermoacoustic tomographic (MTT) imaging. Phys. Med. Biol. https://doi.org/10.1088/1361-6560/abf954 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  228. Yan, A. et al. Microwave-induced thermoacoustic tomography through an adult human skull. Med. Phys. 46, 1793–1797 (2019).

    Article  PubMed  Google Scholar 

  229. Ji, Z., Fu, Y. & Yang, S. H. Microwave-induced thermoacoustic imaging for early breast cancer detection. J. Innov. Opt. Heal. Sci. 6, 1350001 (2013).

    Article  Google Scholar 

  230. Ku, G. & Wang, L. H. V. Scanning microwave-induced thermoacoustic tomography: signal, resolution, and contrast. Med. Phys. 28, 4–10 (2001).

    Article  CAS  PubMed  Google Scholar 

  231. Ku, G. et al. Thermoacoustic and photoacoustic tomography of thick biological tissues toward breast imaging. Technol. Cancer Res. Treat. 4, 559–565 (2005).

    Article  PubMed  Google Scholar 

  232. Liang, B. Y. et al. Acoustic impact of the human skull on transcranial photoacoustic imaging. Biomed. Opt. Express 12, 1512–1528 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  233. Na, S. et al. Transcranial photoacoustic computed tomography based on a layered back-projection method. Photoacoustics 20, 100213 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  234. Mohammadi, L., Behnam, H., Tavakkoli, J. & Avanaki, K. Skull acoustic aberration correction in photoacoustic microscopy using a vector space similarity model: a proof-of-concept simulation study. Biomed. Opt. Express 11, 5542–5556 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  235. Mitsuhashi, K., Wang, L. H. V. & Anastasio, M. A. in Proceedings of SPIE. Vol. 9323: Photons Plus Ultrasound: Imaging and Sensing 2015 (eds Oraevsky, A. A. & Wang, L. V.) 9323 3B (SPIE, 2015).

  236. Hosseinaee, Z., Le, M., Bell, K. & Reza, P. H. Towards non-contact photoacoustic imaging [review]. Photoacoustics 20, 100207 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  237. Bell, K. et al. Reflection-mode virtual histology using photoacoustic remote sensing microscopy. Sci. Rep. 10, 19121 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Cox, B., Laufer, J. G., Arridge, S. R. & Beard, P. C. Quantitative spectroscopic photoacoustic imaging: a review. J. Biomed. Opt. 17, 061202 (2012).

    Article  PubMed  Google Scholar 

  239. Tzoumas, S. et al. Eigenspectra optoacoustic tomography achieves quantitative blood oxygenation imaging deep in tissues. Nat. Commun. 7, 12121 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  240. Bauer, A. Q., Nothdurft, R. E., Erpelding, T. N., Wang, L. H. V. & Culver, J. P. Quantitative photoacoustic imaging: correcting for heterogeneous light fluence distributions using diffuse optical tomography. J. Biomed. Opt. 16, 096016 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  241. Kirillin, M., Perekatova, V., Turchin, I. & Subochev, P. Fluence compensation in raster-scan optoacoustic angiography. Photoacoustics 8, 59–67 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  242. Jeng, G. S. et al. Real-time interleaved spectroscopic photoacoustic and ultrasound (PAUS) scanning with simultaneous fluence compensation and motion correction. Nat. Commun. 12, 716 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Manwar, R., Kratkiewicz, K. & Avanaki, K. Overview of ultrasound detection technologies for photoacoustic imaging. Micromachines 11, 692 (2020).

    Article  PubMed Central  Google Scholar 

  244. Na, S. & Wang, L. H. V. Photoacoustic computed tomography for functional human brain imaging [invited]. Biomed. Opt. Express 12, 4056–4083 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  245. Monchalin, J.-P. Optical detection of ultrasound. IEEE Trans. UFFC 33, 485–499 (1986).

    Article  CAS  Google Scholar 

  246. Wang, K., Su, R., Oraevsky, A. A. & Anastasio, M. A. Investigation of iterative image reconstruction in three-dimensional optoacoustic tomography. Phys. Med. Biol. 57, 5399–5423 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  247. Hauptmann, A. & Cox, B. Deep learning in photoacoustic tomography: current approaches and future directions. J. Biomed. Opt. 25, 112903 (2020).

    Article  CAS  PubMed Central  Google Scholar 

  248. Davoudi, N., Dean-Ben, X. L. & Razansky, D. Deep learning optoacoustic tomography with sparse data. Nat. Mach. Intell. 1, 453–460 (2019).

    Article  Google Scholar 

  249. Bohndiek, S. et al. in Proceedings of SPIE. Vol. 10878: Photons Plus Ultrasound: Imaging and Sensing 2019 (eds Oraevsky, A. A. & Wang, L. V.) 10878 1N (SPIE, 2019).

  250. IEEE International Committee on Electromagnetic Safety (SCC39). IEEE standard for safety levels with respect to human exposure to radio frequency electromagnetic fields, 3 kHz to 300 GHz. IEEE Std C95.1 (IEEE, 2005).

Download references

Acknowledgements

The authors thank R. Cao for useful discussions. The authors are also grateful to J. Ballard, D. Garrett and J. Olick-Gibson for close reading of the paper.

Author information

Authors and Affiliations

Authors

Contributions

Both authors made substantial contributions to all aspects of the preparation of this manuscript.

Corresponding author

Correspondence to Lihong V. Wang.

Ethics declarations

Competing interests

L.V.W. has a financial interest in Microphotoacoustics, Inc., CalPACT, LLC and Union Photoacoustic Technologies, Ltd., which, however, did not support this work. L.L. declares no competing interests.

Peer review

Peer review information

Nature Reviews Clinical Oncology thanks the anonymous reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, L., Wang, L.V. The emerging role of photoacoustic imaging in clinical oncology. Nat Rev Clin Oncol 19, 365–384 (2022). https://doi.org/10.1038/s41571-022-00615-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41571-022-00615-3

This article is cited by

Search

Quick links

Nature Briefing: Cancer

Sign up for the Nature Briefing: Cancer newsletter — what matters in cancer research, free to your inbox weekly.

Get what matters in cancer research, free to your inbox weekly. Sign up for Nature Briefing: Cancer