Combined Monte Carlo and k-Wave Simulations for Reconstruction of Blood Oxygen Saturation in Optoacoustics: A Pilot Study

Valeriya Perekatova orcid (Login required)
Institute of Applied Physics RAS, Nizhny Novgorod, Russia

Daria Kurakina orcid
Institute of Applied Physics RAS, Nizhny Novgorod, Russia

Aleksandr Khilov orcid
Institute of Applied Physics RAS, Nizhny Novgorod, Russia

Mikhail Kirillin orcid
Institute of Applied Physics RAS, Nizhny Novgorod, Russia


Paper #3562 received 10 Nov 2022; revised manuscript received 7 Dec 2022; accepted for publication 12 Dec 2022; published online 24 Dec 2022.

DOI: 10.18287/JBPE22.08.040511

Abstract

Optoacoustic (OA) imaging of biological tissues is a modern technique allowing for three-dimensional blood oxygen saturation mapping based on OA spectroscopy data. Since biological tissues are optically inhomogeneous and the spatial distribution of optical parameters within a biological tissue is a priori unknown, Monte Carlo simulation technique is traditionally used to estimate the distribution of probing illumination within tissues in quantitative OA reconstruction. Currently, machine learning techniques are actively employed for reconstructing 3D distribution of blood oxygen saturation or estimating optical properties of biological tissues based on training datasets. In this paper, systemic calculations of synthetic OA images of a medium with embedded vessel-like structures were performed to create a training dataset for machine learning employing combined application of the Monte Carlo technique for direct solution of optical problem and difference-space pseudo-spectral approach implemented through k-Wave Toolbox calculations for the acoustical part. The calculations were performed for probing wavelengths of 532 nm, 658 nm and 1064 nm, which are commonly employed in spectral OA imaging. Simulated OA data for different orientation, diameter and embedding depth of blood vessels allows analyzing the effect of these parameters on the formation of OA image and the reconstruction of blood oxygen saturation. The ratio of OA signals corresponding to probing wavelengths of 658 nm and 1064 nm was employed for simple reconstruction of blood oxygen saturation in silico for different vessel geometries with the precision of < 3–15% for the most of blood vessels diameters and embedding depths and the range of blood oxygen saturation values ≥ 0.8. The obtained set of synthetic OA data has high potential as a training set for employment in machine learning techniques aiming at mapping blood oxygenation based on spectral OA data.

Keywords

optoacoustic imaging; Monte Carlo modeling; k-Wave modeling; blood oxygen saturation mapping

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References


1. C. Menon, D. L. Fraker, “Tumor oxygenation status as a prognostic marker,” Cancer Letters 221(2), 225–235 (2005).

2. C. Zhou, R. Choe, N. S. Shah, T. Durduran, G. Yu, A. Durkin, D. Hsiang, R. Mehta, J. A. Butler, and A. E. Cerussi, “Diffuse optical monitoring of blood flow and oxygenation in human breast cancer during early stages of neoadjuvant chemotherapy,” Journal of Biomedical Optics 12(5), 051903 (2007).

3. A. A. Tandara, T. A. Mustoe, “Oxygen in wound healing—more than a nutrient,” World Journal of Surgery 28, 294–300 (2004).

4. A. Orlova, Y. Perevalova, K. Pavlova, N. Orlinskaya, A. Khilov, D. Kurakina, M. Shakhova, M. Kleshnin, E. Sergeeva, and I. Turchin, “In Diffuse optical spectroscopy monitoring of experimental tumor oxygenation after red and blue light photodynamic therapy,” Photonics 9(1), 19 (2022).

5. C. Balas, “Review of biomedical optical imaging—a powerful, non-invasive, non-ionizing technology for improving in vivo diagnosis,” Measurement Science and Technology 20(10), 104020 (2009).

6. A. P. Dhawan, B. D’Alessandro, and X. Fu, “Optical imaging modalities for biomedical applications,” IEEE Reviews in Biomedical Engineering 3, 69–92 (2010).

7. T. Durduran, G. Yu, M. G. Burnett, J. A. Detre, J. H. Greenberg, J. Wang, C. Zhou, and A. G. Yodh, “Diffuse optical measurement of blood flow, blood oxygenation, and metabolism in a human brain during sensorimotor cortex activation,” Optics Letters 29(15), 1766–1768 (2004).

8. S. E. Boebinger, R. O. Brothers, S. Bong, B. Sanders, C. McCracken, L. H. Ting, and E. M. Buckley, “Diffuse optical spectroscopy assessment of resting oxygen metabolism in the leg musculature,” Metabolites 11(8), 496 (2021).

9. D. Kurakina, V. Perekatova, E. Sergeeva, A. Kostyuk, I. Turchin, and M. Kirillin, “Probing depth in diffuse reflectance spectroscopy of biotissues: A monte carlo study,” Laser Physics Letters 19, 035602 (2022).

10. A. Orlova, M. Y. Kirillin, A. Volovetsky, N. Y. Shilyagina, and E. Sergeeva, G. Y. Golubiatnikov, and I. Turchin, “Diffuse optical spectroscopy monitoring of oxygen state and hemoglobin concentration during skbr-3 tumor model growth,” Laser Physics Letters 14, 015601 (2016).

11. A. F. Khan, F. Zhang, H. Yuan, and L. Ding, “Brain-wide functional diffuse optical tomography of resting state networks,” Journal of Neural Engineering 18, 046069 (2021).

12. J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” Journal of Cerebral Blood Flow & Metabolism 23(8), 911–924 (2003).

13. L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. I. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).

14. E. Liapis, A. Karlas, U. Klemm, and V. Ntziachristos, “Chemotherapeutic effects on breast tumor hemodynamics revealed by eigenspectra multispectral optoacoustic tomography (emsot),” Theranostics 11(16), 7813 (2021).

15. A. Orlova, M. Sirotkina, E. Smolina, V. Elagin, A. Kovalchuk, I. Turchin, and P. Subochev, “Raster-scan optoacoustic angiography of blood vessel development in colon cancer models,” Photoacoustics 13, 25–32 (2019).

16. P. Subochev, E. Smolina, E. Sergeeva, M. Kirillin, A. Orlova, D. Kurakina, D. Emyanov, and D. Razansky, “Toward whole-brain in vivo optoacoustic angiography of rodents: Modeling and experimental observations,” Biomedical Optics Express 11(3), 1477–1488 (2020).

17. L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nature Photonics 3, 503–509 (2009).

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

19. X. L. Deán‐Ben, D. Razansky, “Optoacoustic imaging of the skin,” Experimental Dermatology 30, 1598–1609 (2021).

20. V. Perekatova, P. Subochev, M. Y. Kirillin, E. Sergeeva, D. Kurakina, A. Orlova, A. Postnikova, and I. Turchin, “Quantitative techniques for extraction of blood oxygenation from multispectral optoacoustic measurements,” Laser Physics Letters 16, 116201 (2019).

21. M. Schwarz, A. Buehler, J. Aguirre, and V. Ntziachristos, “Three‐dimensional multispectral optoacoustic mesoscopy reveals melanin and blood oxygenation in human skin in vivo,” Journal of Biophotonics 9, 55–60 (2016).

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

23. J. Gröhl, M. Schellenberg, K. Dreher, and L. Maier-Hein, “Deep learning for biomedical photoacoustic imaging: A review,” Photoacoustics 22, 100241 (2021).

24. H. Deng, H. Qiao, Q. Dai, and C. Ma, “Deep learning in photoacoustic imaging: A review,” Journal of Biomedical Optics 26(4), 040901 (2021).

25. C. Yang, H. Lan, F. Gao, and F. Gao, “Review of deep learning for photoacoustic imaging,” Photoacoustics 21, 100215 (2021).

26. J. Gröhl, T. Kirchner, T. J. Adler, L. Hacker, N. Holzwarth, A. Hernández-Aguilera, M. A. Herrera, E. Santos, S. E. Bohndiek, and L. Maier-Hein, “Learned spectral decoloring enables photoacoustic oximetry,” Scientific Reports 11, 6565 (2021).

27. J. H. Nölke, T. Adler, J. Gröhl, T. Kirchner, L. Ardizzone, C. Rother, U. Köthe, and L. Maier-Hein, “Invertible neural networks for uncertainty quantification in photoacoustic imaging,” Bildverarbeitung Für Die Medizin 2021, 330–335 (2021).

28. C. Yang, F. Gao, “EDA-Net: Dense aggregation of deep and shallow information achieves quantitative photoacoustic blood oxygenation imaging deep in human breast,” in International Conference on Medical Image Computing and Computer-Assisted Intervention, Springer, Cham, 246–254 (2019).

29. K. Hoffer-Hawlik, G. P. Luke, “Abso2luteu-net: Tissue oxygenation calculation using photoacoustic imaging and convolutional neural networks,” ENGS 88 Honors Thesis (2019).

30. G. P. Luke, K. Hoffer-Hawlik, A. C. Van Namen, and R. Shang, “O-net: A convolutional neural network for quantitative photoacoustic image segmentation and oximetry,” arXiv Preprint, 1911.01935 (2019).

31. C. Bench, A. Hauptmann, and B. T. Cox, “Toward accurate quantitative photoacoustic imaging: Learning vascular blood oxygen saturation in three dimensions,” Journal of Biomedical Optics 25(8), 085003 (2020).

32. L. Wang, S. L. Jacques, and L. Zheng, “Mcml—monte carlo modeling of light transport in multi-layered tissues,” Computer Methods and Programs in Biomedicine 47(2), 131–146 (1995).

33. M. Kirillin, A. Khilov, D. Kurakina, A. Orlova, V. Perekatova, V. Shishkova, A. Malygina, A. Mironycheva, I. Shlivko, S. Gamayunov, I. Turchin, and E. Sergeeva, “Dual-wavelength fluorescence monitoring of photodynamic therapy: From analytical models to clinical studies,” Cancers 13(22), 5807 (2021).

34. A. V. Gorshkov, M. Y. Kirillin, “Acceleration of monte carlo simulation of photon migration in complex heterogeneous media using intel many-integrated core architecture,” Journal of Biomedical Optics 20(8), 085002 (2015).

35. V. Perekatova, S. Nemirova, A. Orlova, M. Kirillin, A. Kurnikov, K. Pavlova, A. Khilov, A. Kovalchuk, and P. Subochev, “Three-dimensional dual-wavelength optoacoustic angiography reveals arteriovenous anastomoses,” Laser Physics Letters 18, 045601 (2021).

36. V. Perekatova, P. Subochev, M. Kleshnin, and I. Turchin, “Optimal wavelengths for optoacoustic measurements of blood oxygen saturation in biological tissues,” Biomedical Optics Express 7(10), 3979–3995 (2016).

37. N. Bosschaart, G. J. Edelman, M. C. Aalders, T. G. van Leeuwen, and D. J. Faber, “A literature review and novel theoretical approach on the optical properties of whole blood,” Lasers in Medical Science 29, 453–479 (2014).

38. T. Kono, J. Yamada, “In vivo measurement of optical properties of human skin for 450–800 nm and 950–1600 nm wavelengths,” International Journal of Thermophysics 40, 51 (2019).

39. B. E. Treeby, B. T. Cox, “K-wave: Matlab toolbox for the simulation and reconstruction of photoacoustic wave fields,” Journal of Biomedical Optics 15(2), 021314 (2010).

40. I. Turchin, S. Bano, M. Kirillin, A. Orlova, V. Perekatova, V. Plekhanov, E. Sergeeva, D. Kurakina, A. Khilov, A. Kurnikov, P. Subochev, M. Shirmanova, A. Komarova, D. Yuzhakova, A. Gavrina, S. Mallidi, and T. Hasan, “Combined fluorescence and optoacoustic imaging for monitoring treatments against ct26 tumors with photoactivatable liposomes,” Cancers 14(1), 197 (2021).

41. V. Perekatova, M. Kirillin, S. Nemirova, A. Orlova, A. Kurnikov, A. Khilov, K. Pavlova, V. Kazakov, V. Vildanov, I. Turchin, and P. Subochev, “Quantitative characterization of age-related changes in peripheral vessels of a human palm using raster-scan optoacoustic angiography,” Photonics 9(7), 482 (2022).

42. P. Subochev, “Cost-effective imaging of optoacoustic pressure, ultrasonic scattering, and optical diffuse reflectance with improved resolution and speed,” Optics Letters 41(5), 1006-1009 (2016).

43. V. V. Perekatova, M. Y. Kirillin, I. V. Turchin, and P. V. Subochev, “Combination of virtual point detector concept and fluence compensation in acoustic resolution photoacoustic microscopy,” Journal of Biomedical Optics 23(9), 091414 (2018).

44. V. Perekatova, M. Kirillin, P. Subochev, A. Kurnikov, A. Khilov, A. Orlova, D. Yuzhakova, and I. Turchin, “Quantification of microvasculature parameters based on optoacoustic angiography data,” Laser Physics Letters 18, 035602 (2021).






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