A new method of intraoperative assessment of the dynamics of cortical blood flow using imaging photoplethysmography

Background. Intraoperative assessment of changes in cerebral blood flow is an important component of objective quality control of surgical treatment of cerebral artery aneurysms. Various techniques have been tried to solve this task, but they all have their drawbacks, which forces us to look for new ways of blood flow monitoring. We propose to use the technology of imaging photoplethysmography (IPPG) – a technically simple, contactless, safe and cheap optical method for assessing the perfusion of biological tissues.
Aim. To demonstrate the possibility of using IPPG to assess the dynamics of cerebral blood flow parameters during aneurysm clipping surgery, as well as to identify early changes in blood supply to the cerebral cortex.
Materials and methods. The study was carried out during six surgeries of clipping aneurysms of the anterior part of the Willis’s circle, both in the acute stage of rupture (n = 1) and in a planned manner (n = 5). The IPPG system, which is an LED illuminator in a single unit with a digital video camera, was located on a tripod 25 cm from the intervention zone. During each operation, two one-minute recordings of the illuminated surface of the cerebral cortex were performed: after dissection of the dura mater and before its suturing at the end of the main stage of the intervention. To improve the measurement accuracy, video frames of the studied area were recorded synchronously with the registration of an electrocardiogram. After recording, two IPPG parameters were calculated and compared: the amplitude of the pulsatile component and the pulse wave transit time. Thereafter, the obtained data were compared with the results of computed tomography. Statistical analysis was performed using pairwise comparison tests in the GraphPad Prism software package.
Results. Clipping of cerebral vessel aneurysms are accompanied by significant changes in the parameters of cerebral blood flow. Analysis of the data for all patients revealed significant differences in IPPG parameters before and after surgery, namely, statistically significant increase in amplitude of the pulsatile component (n = 3) and decrease in pulse wave transit time (n = 5). The absence of significant changes in both parameters was found only in one patient who had mechanical damage in the cortex in the region of video recording.
Conclusion. The IPPG system is capable to quantify changes in blood supply to the cortex during surgical treatment of cerebral artery aneurysms and to identify areas with either increased or decreased blood supply. In-depth studies are required to obtain additional markers of the postoperative state of cerebral blood flow.

1. Fredrickson V.L., Russin J.J., Strickland B.A. et al. Intraoperative imaging for vascular lesions. Neurosurg Clin N Am 2017;28(4):603–13. DOI: 10.1016/j.nec.2017.05.011

2. Kakucs C., Florian I.A., Ungureanu G., Florian I.S. Fluorescein angiography in intracranial aneurysm surgery: a helpful method to evaluate the security of clipping and observe blood flow. World Neurosurg 2017;105:406–11. DOI: 10.1016/j.wneu.2017.05.172

3. Kazmi S.M.S., Richards L.M., Schrandt C.J. et al. Expanding applications, accuracy, and interpretation of laser speckle contrast imaging of cerebral blood flow. J Cereb Blood Flow Metab 2015;35:1076–84. DOI: 10.1038/jcbfm.2015.84

4. Shapey J., Xie Y., Nabavi E. et al. Intraoperative multispectral and hyperspectral label-free imaging: a systematic review of in vivo clinical studies. J Biophotonics 2019;12(9):e201800455. DOI: 10.1002/jbio.201800455

5. Mamontov O.V., Shcherbinin A.V., Romashko R.V., Kamshilin A.A. Intraoperative imaging of cortical blood flow by camera-based photoplethysmography at green light. Appl Sci 2020;10(18):6192. DOI: 10.3390/app10186192

6. Volynsky M.A., Mamontov O.V., Osipchuk A.V. et al. Study of cerebrovascular reactivity to hypercapnia by imaging photoplethysmography to develop a method for intraoperative assessment of the brain functional reserve. Biomed Opt Express 2022;13(1):184–96. DOI: 10.1364/BOE.443477

7. Sokolov A.Y., Volynsky M.A., Zaytsev V.V. et al. Advantages of imaging photoplethysmography for migraine modeling: new optical markers of trigemino-vascular activation in rats. J Headache Pain 2021;22(1):18. DOI: 10.1186/s10194-021-01226-6

8. Mamontov O.V., Sokolov A.Y., Volynsky M.A. et al. Animal model of assessing cerebrovascular functional reserve by imaging photoplethysmography. Sci Rep 2020;10(1):19008. DOI: 10.1038/s41598-020-75824-w

9. Sokolov A.Y., Volynsky M.A., Potapenko A.V. et al. Duality in response of intracranial vessels to nitroglycerin revealed in rats by imaging photoplethysmography. Sci Rep 2023;13:11928. DOI: 10.1038/s41598-023-39171-w

10. Lyubashina O.A., Mamontov O.V., Volynsky M.A. et al. Contactless assessment of cerebral autoregulation by photoplethysmographic imaging at green illumination. Front Neurosci 2019;13:1235. DOI: 10.3389/fnins.2019.01235

11. Hertzman A.B., Spealman C.R. Observations on the finger volume pulse recorded photoelectrically. Am J Physiol 1937;119:334–5. DOI: 10.1152/ajplegacy.1937.119.2.257

12. Reisner A., Shaltis P.A., McCombie D., Asada H.H. Utility of the photoplethysmogram in circulatory monitoring. Anesthesiology 2008;108(5):950–8. DOI: 10.1097/ALN.0b013e31816c89e1

13. Hertzman A.B. The blood supply of various skin areas as estimated by the photoelectric plethysmograph. Am J Physiol 1938;124: 328–40. DOI: 10.1152/ajplegacy.1938.124.2.328

14. Nieveen J., Reichert W.J., van der Slikke L.B. Photoelectric plethysmography using reflected light. Cardiologia (Basel) 1956;29(3):160–73. DOI: 10.1159/000165601

15. Roberts V.C. Photoplethysmography-fundamental aspects of the optical properties of blood in motion. Trans Inst Meas Control 1982;4:101–6. DOI: 10.1177/014233128200400205

16. Verkruysse W., Svaasand L.O., Nelson J.S. Remote plethysmographic imaging using ambient light. Opt Express 2008;16(26):21434–45. DOI: 10.1364/OE.16.021434

17. Maeda Y., Sekine M., Tamura T. The advantages of wearable green reflected photoplethysmography. J Med Syst 2011;35(5):829–50. DOI: 10.1007/s10916-010-9506-z

18. Kamshilin A.A., Miridonov S., Teplov V. et al. Photoplethysmographic imaging of high spatial resolution. Biomed Opt Express 2011;2(4):996–1006. DOI: 10.1364/BOE.2.000996

19. Fallow B.A., Tarumi T., Tanaka H. Influence of skin type and wavelength on light wave reflectance. J Clin Monit Comput 2013;27:313–7. DOI: 10.1007/s10877-013-9436-7

20. Anderson R.R., Parrish J.A. The optics of human skin. J Invest Dermatol 1981;77(1):13–9. DOI: 10.1111/1523-1747.ep12479191

21. Bashkatov A.N., Genina E.A., Kochubey V.I., Tuchin V.V. Optical properties of human skin, subcutaneous and mucous tissues in the wavelength range from 400 to 2000 nm. J Phys D Appl Phys 2005;38(15):2543–55. DOI: 10.1088/0022-3727/38/15/004

22. Kamshilin A.A., Nippolainen E., Sidorov I.S. et al. A new look at the essence of the imaging photoplethysmography. Sci Rep 2015;5:10494. DOI: 10.1038/srep10494

23. Kamshilin A.A., Krasnikova T.V., Volynsky M.A. et al. Alterations of blood pulsations parameters in carotid basin due to body position change. Sci Rep 2018;8(1):13663. DOI: 10.1038/s41598-018-32036-7

24. Kamshilin A.A., Mamontov O.V. Imaging photoplethysmography and its applications. In: Photoplethysmography. Technology, signal analysis and applications. Ed. by J. Allen, P.A. Kyriacou. Academic Press, 2022. Pp. 439–468. DOI: 10.1016/B978-0-12-823374-0.00014-1

25. Sidorov I.S., Volynsky M.A., Kamshilin A.A. Influence of polarization filtration on the information readout from pulsating blood vessels. Biomed Opt Express 2016;7(7):2469–74. DOI: 10.1364/BOE.7.002469

26. Kashchenko V.A., Zaytsev V.V., Ratnikov V.A., Kamshilin A.A. Intraoperative visualization and quantitative assessment of tissue perfusion by imaging photoplethysmography: comparison with ICG fluorescence angiography. Biomed Opt Express 2022;13(7):3954–66. DOI: 10.1364/BOE.462694

27. Kearney J.K., Thompson W.B., Boley D.L. Optical flow estimation: an error analysis of gradient-based methods with local optimization. IEEE Trans Pattern Anal Mach Intell 1987:9(2):229–44. DOI: 10.1109/TPAMI.1987.4767897

28. Allen J. Photoplethysmography and its application in clinical physiological measurement. Physiol Meas 2007;28:R1–R39. DOI: 10.1088/0967-3334/28/3/R01

29. Lima A.P., Beelen P., Bakker J. Use of a peripheral perfusion index derived from the pulse oximetry signal as a noninvasive indicator of perfusion. Crit Care Med 2002;30:1210–3.DOI: 10.1097/00003246-200206000-00006

30. Zaramella P., Freato F., Quaresima V. et al. Foot pulse oximeter perfusion index correlates with calf muscle perfusion measured by near-infrared spectroscopy in healthy neonates. J Perinatol 2005;25:417–22. DOI: 10.1038/sj.jp.7211328