neurosurgeryНейрохирургияRussian journal of neurosurgery1683-32952587-7569Издательский дом "МедИНК"10.17650/1683-3295-2024-26-3-43-56neurosurgery-1570Research ArticleОРИГИНАЛЬНАЯ РАБОТАORIGINAL REPORTНовый метод интраоперационной оценки динамики кровенаполнения мозга с использованием визуализирующей фотоплетизмографииA new method of intraoperative assessment of the dynamics of cortical blood flow using imaging photoplethysmographyhttps://orcid.org/0000-0003-1870-1270ЩербининА. В.ShcherbininA. V.

Антон Владимирович Щербинин

194291 Санкт-Петербург, пр-кт Культуры, 4

Anton Vladimirovich Shcherbinin

4 Kultury Ave., Saint Petersburg 194291

antoxia@yandex.ruhttps://orcid.org/0000-0003-3366-8376ЗайцевВ. В.ZaytsevV. V.

194291 Санкт-Петербург, пр-кт Культуры, 4;

690041 Владивосток, ул. Радио, 5

4 Kultury Ave., Saint Petersburg 194291;

5 Radio St., Vladivostok 690041

https://orcid.org/0000-0002-1317-2683НипполайненЭ. А.NippolainenE. A.

690041 Владивосток, ул. Радио, 5

5 Radio St., Vladivostok 690041

https://orcid.org/0000-0002-6141-486XСоколовА. Ю.SokolovA. Yu.

197022 Санкт-Петербург, ул. Льва Толстого, 6–8;

199034 Санкт-Петербург, Васильевский остров, наб. Макарова, 6;

195271 Санкт-Петербург, Кондратьевский пр-кт, 72 лит. А

6–8 L’va Tolstogo St., Saint Petersburg 197022;

6 Makarova Emb., Saint Petersburg 199034;

72А Kondratyevsky Ave., Saint Petersburg 195271

 

 

https://orcid.org/0000-0003-2506-9736КамшилинА. А.KamshilinA. A.

194291 Санкт-Петербург, пр-кт Культуры, 4;

690041 Владивосток, ул. Радио, 5

4 Kultury Ave., Saint Petersburg 194291;

5 Radio St., Vladivostok 690041

ФГБУ «Северо-Западный окружной научно-клинический центр им. Л.Г. Соколова Федерального медико-биологического агентства»РоссияL.G. Sokolov North-Western District Scientific and Clinical Center, Federal Medical and Biological AgencyRussian FederationФГБУ «Северо-Западный окружной научно-клинический центр им. Л.Г. Соколова Федерального медико-биологического агентства»; ФГБУН «Институт автоматики и процессов управления Дальневосточного отделения Российской академии наук»РоссияL.G. Sokolov North-Western District Scientific and Clinical Center, Federal Medical and Biological Agency; Institute of Automation and Control Processes, Far Eastern Branch, Russian Academy of SciencesRussian FederationФГБУН «Институт автоматики и процессов управления Дальневосточного отделения Российской академии наук»РоссияInstitute of Automation and Control Processes, Far Eastern Branch, Russian Academy of SciencesRussian FederationФГБОУ ВО «Первый Санкт-Петербургский государственный медицинский университет им. акад. И.П. Павлова» Минздрава России; ФГБУН «Институт физиологии им. И.П. Павлова Российской академии наук»; ЧОУВО «Санкт-Петербургский медико-социальный институт»РоссияI.P. Pavlov First St. Petersburg State Medical University, Ministry of Health of Russia; I.P. Pavlov Institute of Physiology, Russian Academy of Sciences; St. Petersburg Medico-Social InstituteRussian Federation2024060920242634356Copyright © Щербинин А.В., Зайцев В.В., Нипполайнен Э.А., Соколов А.Ю., Камшилин А.А., 20242024Щербинин А.В., Зайцев В.В., Нипполайнен Э.А., Соколов А.Ю., Камшилин А.А.Shcherbinin A.V., Zaytsev V.V., Nippolainen E.A., Sokolov A.Y., Kamshilin A.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.therjn.com/jour/article/view/1570

Введение. Интраоперационная оценка изменений церебрального кровотока – важный компонент объективного контроля качества хирургического лечения аневризм артерий головного мозга. Существующие для этой цели аппаратные методики имеют свои недостатки, что заставляет искать новые способы мониторинга кровотока во время операции. Мы предлагаем использовать технологию визуализирующей фотоплетизмографии (ВФПГ) – технически простого, бесконтактного, безопасного и дешевого оптического метода оценки перфузии биологических тканей.Цель работы – продемонстрировать возможность использования ВФПГ для оценки динамики параметров церебрального кровотока во время операции по клипированию аневризмы, а также выявления ранних изменений кровоснабжения коры головного мозга.Материалы и методы. Исследование проведено во время 6 операций клипирования аневризм артерий переднего отдела виллизиевого круга как в острой стадии разрыва (n = 1), так и в плановом порядке (n = 5). Система ВФПГ, представляющая собой светодиодный осветитель в едином блоке с цифровой видеокамерой, располагалась на штативе в 25 см от зоны вмешательства. Во время каждой операции проводили 2 одноминутные записи освещенной поверхности коры мозга – после рассечения твердой мозговой оболочки и перед ее ушиванием по завершении основного этапа интервенции. Для повышения точности измерения запись видеокадров исследуемой области осуществляли синхронно с регистрацией электрокардиограммы. По окончании записи выполняли расчет и сравнение двух ВФПГ-параметров: амплитуды пульсативного компонента и времени прохождения пульсовой волны. После операции полученные данные сопоставляли с результатами компьютерной томографии. Статистический анализ проводили с помощью тестов попарного сравнения в программном пакете GraphPad Prism.Результаты. Операции клипирования аневризм мозговых сосудов сопровождаются значительными изменениями параметров церебрального кровотока. При суммировании данных по всем пациентам были выявлены существенные различия при сравнении ВФПГ-показателей до и после операции, а именно статистически значимые рост амплитуды пульсативного компонента (n = 3) и снижение времени прохождения пульсовой волны (n = 5). Отсутствие достоверных изменений обоих параметров было обнаружено только у 1 пациента с механическим повреждением участка коры в зоне видеосъемки.Заключение. Система ВФПГ позволяет количественно оценивать изменения кровенаполнения коры головного мозга при хирургическом лечении аневризм церебральных артерий и выявлять участки с повышенным и пониженным кровоснабжением. Для получения дополнительных маркеров послеоперационного состояния церебрального кровотока требуются углубленные исследования.

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.

визуализирующая фотоплетизмографияаневризмамикрохирургическое клипированиемозговой кровотоксосуды головного мозганейрохирургияimaging photoplethysmographyaneurysmmicrosurgical clippingcerebral blood flowcerebral vesselsneurosurgeryРабота выполнена при финансовой поддержке Российского научного фонда (грант № 21-15-00265) в части изготовления экспериментального оборудования, разработки программного обеспечения, обработки и анализа данных. Планирование исследований, подготовка пациентов и хирургические вмешательства проводились при финансовой поддержке ФМБА России (рег. № 122031500174-6).The study was carried out with the financial support of the Russian Science Foundation (Grant No. 21-15-00265) in terms of the manufacture of the experimental equipment, software development, and data processing and analysis. Research planning, patient preparation, and surgical interventions were carried out with the financial support of the FMBA of Russia (project No. 122031500174-6).ReferencesFredrickson 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.2017.05.011Fredrickson 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.2017.05.011Kakucs 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.2017.05.172Kakucs 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.2017.05.172Kazmi 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.2015.84Kazmi 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.2015.84Shapey 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.201800455Shapey 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.201800455Mamontov 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/app10186192Mamontov 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/app10186192Volynsky 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.443477Volynsky 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.443477Sokolov 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/s10194-021-01226-6Sokolov 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/s10194-021-01226-6Mamontov 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-wMamontov 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-wSokolov 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-wSokolov 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-wLyubashina 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.2019.01235Lyubashina 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.2019.01235Hertzman A.B., Spealman C.R. Observations on the finger volume pulse recorded photoelectrically. Am J Physiol 1937;119:334–5. DOI: 10.1152/ajplegacy.1937.119.2.257Hertzman A.B., Spealman C.R. Observations on the finger volume pulse recorded photoelectrically. Am J Physiol 1937;119:334–5. DOI: 10.1152/ajplegacy.1937.119.2.257Reisner 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.0b013e31816c89e1Reisner 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.0b013e31816c89e1Hertzman 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.1938.124.2.328Hertzman 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.1938.124.2.328Nieveen J., Reichert W.J., van der Slikke L.B. Photoelectric plethysmography using reflected light. Cardiologia (Basel) 1956;29(3):160–73. DOI: 10.1159/000165601Nieveen J., Reichert W.J., van der Slikke L.B. Photoelectric plethysmography using reflected light. Cardiologia (Basel) 1956;29(3):160–73. DOI: 10.1159/000165601Roberts V.C. Photoplethysmography-fundamental aspects of the optical properties of blood in motion. Trans Inst Meas Control 1982;4:101–6. DOI: 10.1177/014233128200400205Roberts V.C. Photoplethysmography-fundamental aspects of the optical properties of blood in motion. Trans Inst Meas Control 1982;4:101–6. DOI: 10.1177/014233128200400205Verkruysse W., Svaasand L.O., Nelson J.S. Remote plethysmographic imaging using ambient light. Opt Express 2008;16(26):21434–45. DOI: 10.1364/OE.16.021434Verkruysse W., Svaasand L.O., Nelson J.S. Remote plethysmographic imaging using ambient light. Opt Express 2008;16(26):21434–45. DOI: 10.1364/OE.16.021434Maeda 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-zMaeda 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-zKamshilin 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.2.000996Kamshilin 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.2.000996Fallow 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/s10877-013-9436-7Fallow 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/s10877-013-9436-7Anderson R.R., Parrish J.A. The optics of human skin. J Invest Dermatol 1981;77(1):13–9. DOI: 10.1111/1523-1747.ep12479191Anderson R.R., Parrish J.A. The optics of human skin. J Invest Dermatol 1981;77(1):13–9. DOI: 10.1111/1523-1747.ep12479191Bashkatov 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: 10.1088/0022-3727/38/15/004Bashkatov 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: 10.1088/0022-3727/38/15/004Kamshilin 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/srep10494Kamshilin 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/srep10494Kamshilin 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/s41598-018-32036-7Kamshilin 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/s41598-018-32036-7Kamshilin 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/B978-0-12-823374-0.00014-1Kamshilin 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/B978-0-12-823374-0.00014-1Sidorov 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.7.002469Sidorov 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.7.002469Kashchenko 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.462694Kashchenko 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.462694Kearney 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.1987.4767897Kearney 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.1987.4767897Allen J. Photoplethysmography and its application in clinical physiological measurement. Physiol Meas 2007;28:R1–R39. DOI: 10.1088/0967-3334/28/3/R01Allen J. Photoplethysmography and its application in clinical physiological measurement. Physiol Meas 2007;28:R1–R39. DOI: 10.1088/0967-3334/28/3/R01Lima 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: 10.1097/00003246-200206000-00006Lima 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: 10.1097/00003246-200206000-00006Zaramella 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.7211328Zaramella 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

The authors declare that there are no conflicts of interest present.