Age-associated changes in the functional state of microhemocirculation

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Abstract

The microcirculatory bed is a crucial component of the cardiovascular system, at the level of which transcapillary metabolism occurs, which ensures the maintenance of body homeostasis. The analysis of changes in the mechanisms of microcirculation regulation depending on age is directly related to the development of predictive medicine.

Objective: To assess the dynamics of functional changes in microcirculation across different age groups and to identify the mechanisms of microcirculatory regulation in relation to age.

The study involved volunteers (from the city of Semenov) divided into three age groups. Group 1: 18–44 years old, group 2: 45–59 years old, Group 3: 60–74 years old. The work analyzed the normalized characteristics of the rhythms of blood flow fluctuations, studied the microcirculation index, indicators of oxidative and energy metabolism on the laser diagnostic device "LAZMA ST" (NPP "Lazma" LLC, Russia).

The study found that there was a decrease in the amplitudes of the endothelial rhythm (Ae), neurogenic rhythm (An) and heart rate (Ac) in group 2 compared to group 1, which was accompanied by an increase in microcirculation and increased oxidative metabolism. A further increase in perfusion and index of oxidative metabolism in group 3 caused a maximum decrease in the heart rate amplitude (As) and an increase in the endothelial (Ae), neurogenic (An) and myogenic (Am) amplitudes compared with groups 1 and 2. Energy metabolism indicators did not change significantly between the groups.

Thus, as people age there was an increase in the volume of blood entering the microcirculatory bed and an increase in oxidative metabolism, which was accompanied not only by changes in the reactivity of the cardiac component, but also an increase in the importance of local regulatory mechanisms in group 3.

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About the authors

A. V. Deryugina

Institute of Biology and Biomedicine National Research Lobachevsky State University of Nizhny Novgorod

Email: danilovad.a@mail.ru
Russian Federation, Nizhny Novgorod

D. D. Danilova

Institute of Biology and Biomedicine National Research Lobachevsky State University of Nizhny Novgorod

Author for correspondence.
Email: danilovad.a@mail.ru
Russian Federation, Nizhny Novgorod

Y. A. Starateleva

Institute of Biology and Biomedicine National Research Lobachevsky State University of Nizhny Novgorod

Email: danilovad.a@mail.ru
Russian Federation, Nizhny Novgorod

M. N. Talamanova

Institute of Biology and Biomedicine National Research Lobachevsky State University of Nizhny Novgorod

Email: danilovad.a@mail.ru
Russian Federation, Nizhny Novgorod

References

  1. Guven G, Hilty MP, Ince C (2020) Microcirculation: physiology, pathophysiology, and clinical application. Blood Purif 49(1–2): 143–150. https://doi.org/10.1159/000503775
  2. Муравьев АВ, Михайлов ПВ, Тихомирова ИА (2017) Микроциркуляция и гемореология: точки взаимодействия. Регионар кровообращ микроциркул 16(2): 90–100. [Muravyov AV, Mikhailov PV, Tikhomirova IA (2017) Microcirculation and hemorheology: points of interaction. Region Blood Circul Microcircul 16(2): 90–100. (In Russ)]. https://doi.org/10.24884/1682-6655-2017-16-2-90-100
  3. Плотников БМ, Алиев ОИ, Анищенко АМ, Сидехменова АВ, Шаманаев АЮ, Фомина ТИ (2016) Параметры капиллярной сети коры головного мозга крыс линии SHR в периоды развития артериальной гипертензии и стабильно высокого артериального давления. Рос физиол журн им ИМ Сеченова 102(5): 558–566. [Plotnikov MB, Aliev OI, Anishchenko AM, Sidekhmenova AB, Shamanaev AY, Fomina TI (2016) Parameters of cerebral cortex capillary network in shr rats during the development of arterial hypertension and stable high blood pressure. Russ J Physiol 102(5): 558–566. (In Russ)].
  4. Бархатов ИВ (2013) Оценка системы микроциркуляции крови методом лазерной допплеровской флоуметрии. Клин мед 91(11): 21–27. [Barkhatov IV (2013) Assessment of the microcirculation system by laser Doppler flowmetry. Klin Med (Mosk) 91(11): 21–27. (In Russ)].
  5. Арутюнян АВ, Козина ЛС (2009) Механизмы свободнорадикального окисления и его роль в старении. Успехи геронтол 22(1): 104–116. [Arutiunian AV, Kozina LS (2009) Mechanisms of free radical oxidation and its role in aging. Adv Gerontol 22(1): 104–116. (In Russ)].
  6. Михайлов ПВ, Муравьев АВ, Осетров ИА, Муравьев АА (2019) Возрастные изменения микроциркуляции: роль регулярной физической активности. Науч результ биомед исследов 5(3): 82–91. [Mikhailov PV, Muravyov AV, Osetrov IA, Muravyov AА (2019) Age-related changes in microcirculation: the role of regular physical activity. Res Results Biomed 5(3): 82–91. (In Russ)]. https://doi.org/10.18413/2658-6533-2019-5-3-0-9
  7. Федорович АА (2010) Функциональное состояние регуляторных механизмов микроциркуляторного кровотока в норме и при артериальной гипертензии по данным лазерной допплеровской флоуметрии. Регионар кровообращ микроциркул 9(1): 49–60. [Fedorovich AA (2010) The functional state of regulatory mechanisms of the microcirculatory blood flow in normal conditions and in arterial hypertension according to laser doppler flowmetry. Region Blood Circulat Microcirculat 9(1): 49–60. (In Russ)]. https://doi.org/10.24884/1682-6655-2010-9-1-49-60
  8. Крупаткин АИ (2007) Лазерная доплеровская флоуметрия: международный опыт и распространенные ошибки. Регионар кровообращ микроциркул 6(21): 90–92. [Krupatkin AI (2007) Laser Doppler flowmetry: international experience and common mistakes. Region Blood Circulat Microcirculat 6(21): 90–92. (In Russ)].
  9. Kralj L, Lenasi H (2023) Wavelet analysis of laser Doppler microcirculatory signals: Current applications and limitations. Front Physiol 20(13): 1076445. https://doi.org/10.3389/fphys.2022.1076445
  10. Huang SJY, Wang X, Halvorson BD, Bao Y, Frisbee SJ, Frisbee JC, Goldman D (2024) Laser Doppler Fluximetry in Cutaneous Vasculature: Methods for Data Analyses. J Vasc Res 61(4): 197–211. https://doi.org/10.1159/000538718
  11. Martini R, Bagno A (2018) The wavelet analysis for the assessment of microvascular function with the laser Doppler fluxmetry over the last 20 years. Looking for hidden informations. Clin Hemorheol Microcirc 70(2): 213–229. https://doi.org/10.3233/CH-189903
  12. Theodossiou A, Hu L, Wang N, Nguyen U, Walsh AJ (2021) Autofluorescence Imaging to Evaluate Cellular Metabolism. J Vis Exp 177. https://doi.org/10.3791/63282
  13. Skala M, Ramanujam N (2010) Multiphoton redox ratio imaging for metabolic monitoring in vivo. Methods Mol Biol 594: 155–162. https://doi.org/10.1007/978-1-60761-411- 1_11
  14. Corpas FJ, Barroso JB (2014) NADPH-generating dehydrogenases: their role in the mechanism of protection against nitro-oxidative stress induced by adverse environmental conditions. Front Environ Sci 2. https://doi.org/10.3389/fenvs.2014.00055
  15. Staniszewski K, Audi SH, Sepehr R, Jacobs ER, Ranji M (2013) Surface fluorescence studies of tissue mitochondrial redox state in isolated perfused rat lungs. Ann Biomed Eng 41(4): 827–836. https://doi.org/10.1007/s10439-012-0716-z
  16. Абрамович СГ, Машанская АВ, Дробышев ВА, Долбилкин АЮ (2013) Вариабельность типов микроциркуляции у здоровых людей и больных артериальной гипертонией. Сибирск мед журн 2: 11. [Abramovich SG, Mashanskaya АV, Drobyshev VA, Dolbilkin АY (2013) Variability of microcirculation types at healthy people and patients with arterial hypertonia. J Siber Med 2: 11. (In Russ)].
  17. Раваева МЮ, Чуян ЕН (2018) Адаптация тканевой микрогемодинамики к условиям комбинации стрессовых факторов. Учен записки Крымск федер универ им ВИ Вернадского Биология Химия 4(70)(4): 165–179. [Ravaeva MYu, Chuyan EN (2018) Adaptation of tissue microhemodynamics to the conditions of combination of stress factors. Scient notes of Taurida Vernadsky National Univer Ser: Biol Chem 4(70)(4): 165–179. (In Russ)].
  18. Подзолков ВИ, Драгомирецкая НА, Беляев ЮГ, Русинов ИС (2021) Показатели микроциркуляции сосудов кожи у пациентов с хронической сердечной недостаточностью с различной степенью систолической дисфункции левого желудочка. Кардиоваск терапия и профилакт 20(7): 2989. [Podzolkov VI, Dragomiretskaya NA, Beliaev YuG, Rusinov IS (2021) Skin microcirculation in patients with heart failure with different left ventricular systolic dysfunction. Cardiovasc Therapy and Prevent 20(7): 2989. (In Russ)]. https://doi.org/10.15829/1728-8800-2021-2989
  19. Крупаткин АИ, Сидоров ВВ (2005) Лазерная допплеровская флоуметрия микроциркуляции крови. Москва. Медицина. [Krupatkin AI, Sidorov VV (2005) Laser doppler flowmetry of blood microcirculation. Moscow. Meditsina. (In Russ)].
  20. Kvandal P, Stefanovska A, Veber M, Kvernmo HD, Kirkebøen KA (2003) Regulation of human cutaneous circulation evaluated by laser Doppler flowmetry, iontophoresis, and spectral analysis: importance of nitric oxide and prostaglandines. Microvasc Res 65(3): 160–171. https://doi.org/10.1016/s0026-2862(03)00006-2
  21. Бокерия ОЛ, Куулар АМ (2014) Оценка влияния низкоинтенсивных электромагнитных полей на эндотелиальную функцию у больных с хронической сердечной недостаточностью. Сарат науч-мед журн 10(1): 86–92. [Bokeria OL, Kuular AM (2014) Influence of low-intensity electromagnetic fields on endothelial function in patients with chronic heart failure. Saratov J Med Scient Res 10(1): 86–92. (In Russ)].
  22. Li L, Mac-Mary S, Marsaut D, Sainthillier JM, Nouveau S, Gharbi T, de Lacharriere O, Humbert P (2006) Age-related changes in skin topography and microcirculation. Arch Dermatol Res 297(9): 412–416. https://doi.org/10.1007/s00403-005-0628-y
  23. Li L, Mac-Mary S, Sainthillier JM, Nouveau S, de Lacharriere O, Humbert P (2006) Age-related changes of the cutaneous microcirculation in vivo. Gerontology 52(3): 142–153. https://doi.org/10.1159/000091823
  24. Albu M, Seicaru DA, Plesea RM, Mirea OC, Gherghiceanu F, Grigorean VT, Cordos I, Litescu M, Plesea IE, Serbanescu MS (2021) Assessment of the aortic wall histological changes with ageing. Rom J Morphol Embryol 62(1): 85–100. https://doi.org/10.47162/RJME.62.1.08
  25. Rogers WJ, Hu YL, Coast D, Vido DA, Kramer CM, Pyeritz RE, Reichek N (2001) Age-associated changes in regional aortic pulse wave velocity. J Am Coll Cardiol 38(4): 1123–1129. https://doi.org/10.1016/s0735-1097(01)01504-2
  26. Collins JA, Munoz JV, Patel TR, Loukas M, Tubbs RS (2014) The anatomy of the aging aorta. Clin Anat 27(3): 463–466. https://doi.org/10.1002/ca.22384
  27. London GM, Guérin AP, Marchais SJ, Metivier F, Pannier B, Adda H (2003) Arterial media calcification in end-stage renal disease: impact on all-cause and cardiovascular mortality. Nephrol Dial Transplant 18(9): 1731–1740. https://doi.org/10.1093/ndt/gfg414
  28. Pescatore LA, Gamarra LF, Liberman M (2019) Multifaceted Mechanisms of Vascular Calcification in Aging. Arterioscler Thromb Vasc Biol 39(7): 1307–1316. https://doi.org/10.1161/ATVBAHA.118.311576
  29. Donato AJ, Machin DR, Lesniewski LA (2018) Mechanisms of dysfunction in the aging vasculature and role in age-related disease. Circ Res 123(7): 825–848. https://doi.org/10.1161/circresaha.118.312563
  30. Van Bussel FC, van Bussel BC, Hoeks AP, Op't Roodt J, Henry RM, Ferreira I, Vanmolkot FH, Schalkwijk CG, Stehouwer CD, Reesink KD (2015) A control systems approach to quantify wall shear stress normalization by flow-mediated dilation in the brachial artery. PLoS One 10(2): e0115977. https://doi.org/10.1371/journal.pone.0115977
  31. Jaminon A, Reesink K, Kroon A, Schurgers L (2019) The role of vascular smooth muscle cells in arterial remodeling: focus on calcification-related processes. Int J Mol Sci 20: 5694. https://doi.org/10.3390/ijms20225694
  32. Uchimido R, Schmidt EP, Shapiro NI (2019) The glycocalyx: a novel diagnostic and therapeutic target in sepsis. Crit Care 23(1): 16. https://doi.org/10.1186/s13054-018-2292-6
  33. Weinbaum S, Tarbell JM, Damiano ER (2007) The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121–167. https://doi.org/10.1146/annurev.bioeng.9.060906.151959
  34. Литвин ФБ, Голощапова СС, Аверьянов МА, Мартынов СВ, Жигало ВЯ, Аносов ИП (2013) Влияние кратковременного применения экстракта лимонника китайского на микроциркуляцию крови у спортсменов. Вестн Брянск гос универ 4: 120–124. [Litvin FB, Goloshchcapova SS, Averyanov MA, Martinov SV, Jigalo VYa, Anosov IP (2013) The influence of shot-term use of schizandra chinensis (turkz) Baill extract on sportsmen blood microcirculation. Bryansk state univer herald 4: 120–124. (In Russ)]
  35. Муравьев АВ, Ахапкина АА, Михайлов ПВ, Муравьев АА (2014) Микроциркуляция в коже при мышечной нагрузке как модель для изучения общих механизмов изменения микрокровотока. Регионар кровообращ микроциркул 13(2): 64–68. [Muravyov AV, Akhapkina AA, Mikhailov PV, Muravyov AA (2014) Skin microcirculation under muscular exercise as a model for the study of the mechanisms of microcirculatory alterations. Region Blood Circulat Microcirculat 13(2): 64–68. (In Russ)]. https://doi.org/10.24884/1682-6655-2014-13-2-64-68

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2. Fig. 1. Microcirculation indices in different age groups. (a) – amplitude-frequency characteristics of microcirculation in the endothelial (Ae), neurogenic (An), myogenic (Am), respiratory (Ad) and cardiac (Ac) components. (b) – microcirculation index. * p < 0.05, statistical significance in relation to group 1, ** – p < 0.05, statistical significance of group 3 indices in relation to group 2.

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3. Fig. 2. Oxidative and energetic parameters of blood flow in different age groups. (a) – amplitudes of NADH, FAD fluorescence and FAD/NADH redox ratio. (b) – oxidative metabolism parameter. * – p < 0.05, statistical significance in relation to group 1, ** – p < 0.05, statistical significance of parameters of group 3 in relation to group 2.

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4. Fig. 3. Correlation relationships between tissue perfusion and amplitude-frequency characteristics of microcirculation: endothelial (Ae), neurogenic (An), myogenic (Am), respiratory (Ad) and cardiac (Ac) components.

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5. Fig. 4. Correlation dependences of oxidative metabolism on the amplitude-frequency characteristics of microcirculation: endothelial (Ae), neurogenic (An), myogenic (Am), respiratory (Ad) and cardiac (Ac) components.

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