The Amplitude and Frequency Spectrum of Cerebral Blood Flow Fluctuations in Hemorrhagic Shock

Objective: to study the mechanisms of changes in local cerebral blood flows in blood loss and after its replacement.

Material and methods. Experiments were carried out on 24 outbred male rats weighing 400—550 g, anesthetized with nembutal or chloralhydrate. The caudal artery was catheterized to measure blood pressure (BP), to sample and reinfuse blood. Blood flow in the pial vessels of the left parietal region was recorded by laser Doppler flowmetry. Onehour hypovolemic hypotension followed by autoblood reinfusion served as a model. Blood loss volume necessitated maintenance of BP at about 50 mm Hg by 60 minutes of hypotension. The investigators determined the following indicators of local cerebral circulation: microcirculatory index (MI) and relative perfusion units (pf. u); a wavelet method was used to estimate the maximum amplitudes of blood flow fluctuations (flux motions) in the ranges accepted to be correlated with active and passive mechanisms to reulate microcirculation. The data were statistically processed by applying the Statistica 7.0 program. The results were presented as Me (25%; 75%).

Results. According to BP at 60 minutes of blood loss, the animals were divided into 2 groups: 1) more than 50 mm Hg (compensated animals) and 2) less than 50 mm Hg (decompensated ones). The groups did not differ in blood loss amount. At 60 minutes of hypotension, both groups showed diminished cerebral blood flow relative to the outcome with a tendency towards a more marked reduction in the decompensated animals. Throughout the hypotension period, the compensated animals displayed an increase in the amplitude of flux motion in the range of 0.06-0.12 Hz both relative to the outcome and versus the decompensated rats (p<0.05). In the latter, this indicator did not differ from its baseline values throughout the period. After blood reinfusion, all analyzed indicators in the compensated animals did not differ from thebaseline values (p<0.05). The group of decompensated animals was characterized by a poor recovery period, which was reflected by the lower values of BP and MI and tension of compensatory mechanisms for regulation of microcirculation.

Conclusion. With hypovolemic hypotension, the increased amplitude of flux motions in the pial vessels involves the animals' capacity to compensate BP and it is an individual typological feature of microcirculation. The weak ability of the decompensated rats to develop highamplitude flux motions restricts the processes of cerebral circulatory recovery in the reinfusion period.

cerebral blood flow, laser Doppler flowmetry, wavelet analysis, hemorrhagic shock

1. Gutierrez G., Reines H.D., Wulf Gutierrez M.E. Clinical review: hemorrhagic shock. Crit. Care. 2004; 8 (5): 373—381. PMID: 15469601

2. Герасимов Л.В., Карпун Н.А., Пирожкова О.С. Избранные вопросы патогенеза и интенсивного лечения тяжелой сочетанной травмы. Общая реаниматология. 2012; 8 (4): 111—117.

3. Кричевский Л.А., Рыбаков В.Ю., Гусева О.Г., Лямин А.Ю., Харламова И.Е., Магилевец А.И. Ранняя диагностика критических постперфузионных расстройств кровообращения. Общая реаниматология. 2012; 8 (3): 25—30.

4. Donati A., Domizi R., Damiani E., Adrario E., Pelaia P., Ince C. From macrohemodynamic to the microcirculation. Crit. Care Res. Pract. 2013; 2013: 892710. http://dx.doi.org/10.1155/2013/892710. PMID: 23509621

5. Токмакова Т.О., Пермякова С.Ю., Киселева А.В., Шукевич Д.Л., Григорьев Е.В. Мониторинг микроциркуляции в критических состояниях: возможности и ограничения. Общая реаниматология. 2012; 8 (2): 74—78.

6. Косовских А.А., Чурляев Ю.А., Кан С.Л., Лызлов А.Н., Кирсанов Т.В., Вартанян А.Р. Центральная гемодинамика и микроциркуляция при критических состояниях. Общая реаниматология. 2013; 9 (1): 18—22.

7. Tuor U.I., Farrar J.K. Pial vessel caliber and cerebral blood flow during hemorrhage and hypercapnia in the rabbit. Am. J. Physiol. 1984; 247 (1 Pt 2): 40—51. PMID: 6742212

8. Tonnesen J., Pryds A., Larsen E.H., Paulson O.B., Hauerberg J., Knudsen G.M. LaserDoppler flowmetry is valid for measurement of cerebral blood flow autoregulation lower limit in rats. Exp. Physiol. 2005; 90 (3): 349—355. http://dx.doi.org/10.1113/expphysiol.2004.029512. PMID: 15653714

9. Bor-Seng-Shu E., Kita W.S., Figueiredo E.G., Paiva W.S., Fonoff E.T., Teixeira M.J., Panerai R.B. Cerebral hemodynamics: concepts of clinical importance. Arq. Neuropsiquiatr. 2012; 70 (5): 352—356. PMID: 22618788

10. Stefanovska A., Bracic M. Physics of the human cardiovascular system. Contemporary Physics. 1999; 40 (1): 31—35. http://dx.doi.org/10.1080/001075199181693. PMID: 10513128

11. Крупаткин А.И., Сидоров В.В. Лазерная допплеровская флоуметрия микроциркуляции крови. Руководство для врачей. М.: Медицина; 2005: 256.

12. Козлов В.И., Азизов Г.А., Гурова О.А., Литвин Ф.Б. Лазерная допплеровская флоуметрия в оценке состояния и расстройств микроциркуляции крови. Методическое пособие для врачей. М.; 2012: 32.

13. Kuroiwa T., Bonnekoh P., Hossmann K.A. Laser doppler flowmetry in CA1 sector of hippocampus and cortex after transient forebrain ischemia in gerbils. Stroke.1992; 23 (9): 1349—1354. http://dx.doi.org/10.1161/01.STR.23.9.1349. PMID: 1519291

14. Ebel H., Rust D.S., Leschinger A., Ehresmann N., Kranz A., Hoffmann O., Böker D.K. Vasomotion, regional cerebral blood flow and intracranial pressure after induced subarachnoid haemorrhage in rats. Zentralbl. Neurochir. 1996; 57 (3): 150—155. PMID: 8794547

15. Morita Y., Hardebo J.E., Bouskela E. Influence of cerebrovascular sympathetic, parasympathetic, and sensory nerves on autoregulation and spontaneous vasomotion. Acta Physiol. Scand. 1995; 154 (2): 121—130. http://dx.doi.org/10.1111/j.1748—1716.1995.tb09894.x. PMID: 7572208

16. Jones S.C., Radinsky C.R., Furlan A.J., Chyatte D., Perez Trepichio A.D. Cortical NOS inhibition raises the lower limit of cerebral blood flowarterial pressure autoregulation. Am. J. Physiol. 1999; 276 (4 Pt 2): H1253—H1262. PMID: 10199850

17. Александрин В.В. Вейвлет анализ мозгового кровотока у крыс. Регионарное кровообращение и микроциркуляция. 2010; 4 (36): 63—66.

18. Eyre J.A., Essex T.J., Flecknell P.A., Bartholomew P.H., Sinclair J.I. A comparison of measurements of cerebral blood flow in the rabbit using laser Doppler spectroscopy and radionuclide labelled microspheres. Clin. Phys. Physiol. Meas. 1988; 9 (1): 65—74. http://dx.doi.org/10.1088/0143—0815/9/1/006. PMID: 2966027

19. Александрин В.В. Использование метода лазерной допплеровской флоуметрии для определения нижней границы ауторегуляции мозгового кровотока у крыс. Методология флоуметрии. 2000; 4: 139—144.

20. Morita-Tsuzuki Y., Bouskela E., Hardebo J.E. Vasomotion in the rat cerebral microcirculation recorded by laser Doppler flowmetry. Acta Physiol. Scand. 1992; 146 (4): 431—439. http://dx.doi.org/10.1111/j.1748—1716.1992.tb09444.x. PMID: 1492561

21. Li Z., Tam E.W., Kwan M.P., Mak A.F., Lo S.C., Leung M.C. Effects of prolonged surface pressure on the skin blood flowmotions in anaesthetized rats—an assessment by spectral analysis of laser Doppler flowmetry signals. Phys. Med. Biol. 2006; 51 (10): 2681—2694. http://dx.doi.org/10.1088/0031—9155/51/10/020. PMID: 16675876

22. Wan Z., Sun S., Ristagno G., Weil V.H., Tang W. The cerebral microcirculation is protected during experimtntal hemorrhagic shock. Crit. Care Med. 2010; 38 (3): 928—932. http://dx.doi.org/10.

23. /CCM.0b013e3181cd100c. PMID: 20068466

24. du Toit D.F., van Schalkwyk G.D., Wadee S.A., Warren B.L. Neurologic outcome after penetrating extracranial arterial trauma. J. Vasc. Surg. 2003; 38 (2): 257—262. http://dx.doi.org/10.1016/S0741—5214(03)00143—5. PMID: 12891106

25. Werner C., Lu H., Engelhard K., Unbehaun N., Kochs E. Sevoflurane impairs cerebral blood flow autoregulation in rats: reversal by nonselective nitric oxide synthase inhibition. Anesth. Analg. 2005; 101 (2): 509—516. http://dx.doi.org/10.1213/01.ANE.0000160586.71403.A4. PMID: 16037169

26. Aalkjær C., Boedtkjer D., Matchkov V. Vasomotion — what is currently thought? Acta Physiol. (Oxf.). 2011; 202 (3): 253—269. http://dx.doi.org/10.1111/j.1748—1716.2011.02320.x. PMID: 21518271

27. Goldman D., Popel A.S. A computational study of the effect of vasomotion on oxygen transport from capillary networks. J. Theor. Biol. 2001; 209 (2): 189—199. http://dx.doi.org/10.1006/jtbi.2000.2254. PMID: 11401461

28. Sakurai T., Terui N. Effects of sympathetically induced vasomotion on tissue capillary fluid exchange. Am. J. Physiol. Heart Circ. Physiol. 2006; 291 (4): H1761 H1767. http://dx.doi.org/10.1152/ajpheart.

29. 2006. PMID: 16731646

30. Thorn C.T., Kyte H., Slaff D.W., Shore A.C. An association between vasomotion and oxygen extraction. Am. J. Physiol. Heart Circ. Physiol. 2011; 301 (2): H442 H449. http://dx.doi.org/10.1152/ajp-heart.01316.2010. PMID: 21602466

31. Морман Д., Хеллер Л. Физиология сердечно-сосудистой системы. СПб.: Питер; 2000: 256.

32. Неговский В.А., Гурвич А.М., Золотокрылина Е.С. Постреанимационная болезнь. М.: Медицина; 1987: 480.