The effect of selective hypothermia of the cerebral cortex on metabolism in patients with prolonged impairment of consciousness

Abstract

BACKGROUND: Selective craniocerebral hypothermia, used in the acute period of brain damage, ensures the development of positive clinical effects (rapid and persistent reduction of neurological deficit, increased consciousness, and maintenance of normothermy in feverish patients). The safety and efficacy of craniocerebral hypothermia in the acute period of cerebrovascular lesions prompted the use of craniocerebral cooling in patients with chronic disorders of consciousness. For this category of patients, the craniocerebral hypothermia technique has been developed, which requires careful study including its effect on overall metabolism.

AIMS: To determine the nature of the metabolic response to craniocerebral hypothermia procedures in patients in a vegetative state and minimal conscious state.

MATERIALS AND METHODS: A pilot study was conducted from February 3, 2021 until March 3, 2022. This study included 34 patients who were in a state of chronic disorders of consciousness, CRS-R score of <8 (vegetative state and minimally conscious state), after severe brain damage (stroke, 25; brain injury, 5; anoxic brain injuries, 4). Hypothermia was induced using the ATG-01 device, lowering the temperature of the scalp to 4–7°C with a cooling procedure lasting for 120 min. The indirect calorimetry method was conducted before cooling and after 105 min of the craniocerebral hypothermia session. Statistical analysis was performed using the program StatTech v. 2.6.5 (StarTech LLC, Russia).

RESULTS: Craniocerebral cooling provided a decrease in the temperature of the frontal cortex of the large hemispheres already after 30 min from 36.4°C to 34.9±0.41°C in the left hemisphere and 34.7±0.47°C in the right hemisphere. By the 120th minute, the temperature in the left hemisphere reached 34.0±0.40°C, and that in the right hemisphere reached 33.3±0.51°C, decreasing by 2.4°C and 3.1°C, respectively. Subsequently, 30 min after the completion of craniocerebral hypothermia, the brain temperature remained lowered by 0.7°C. Changes in the level of metabolism under the influence of craniocerebral hypothermia were of a multidirectional nature. In 24 patients (70.59%), the resting energy expenditure (REE) index increased to varying degrees by the end of the cooling procedure, and in 10 participants, it decreased. A significant spread of data allowed only a descriptive analysis of the results obtained during a 120-min craniocerebral hypothermia session.

CONCLUSIONS: Chronic disorders of consciousness are largely associated with severe damage of the cerebral cortex. It can be assumed that in patients who reacted with a decrease in REE to the induction of hypothermia, at least metabolic activity in the intact parts of the cerebral cortex was preserved to a certain extent, which may indicate some level of rehabilitation potential. The lack of expression of the reactions of the general metabolism to craniocerebral cooling may be due to the fact that the severe damage to the cerebral cortex excluded the selectivity of hypothermic exposure.

Keywords

craniocerebral hypothermia / metabolism / indirect calorimetry / chronic critical condition / microwave radiothermometry

References

[1] Shevelev OA, Grechko AV, Petrova MV, et al. Therapeutic hypothermia. Moscow: RUDN; 2019. 265 р. (In Russ).

[2] Шевелев О.А., Гречко А.В., Петрова М.В., и др. Терапевтическая гипотермия. Москва: РУДН, 2019. 265 с.

[3] Torosyan BD, Butrov AV, Shevelev OA, et al. Craniocerebral hypothermia is an effective means of neuroprotection in patients with cerebral infarction. Anesthesiol Resuscitation. 2018;(3):58–63. (In Russ). doi: 10.17116/anaesthesiology201803158

[4] Торосян Б.Д., Бутров А.В., Шевелев О.А., и др. Краниоцеребральная гипотермия ― эффективное средство нейропротекции у пациентов с инфарктом мозга // Анестезиология и реаниматология. 2018. № 3. С. 58–63. doi: 10.17116/anaesthesiology201803158

[5] Parugaev KA, Solodov AA, Suryakhin VS, et al. Temperature control in intensive care: current issues. Anesthesiol Resuscitation. 2019;(3):45–55. (In Russ). doi: 10.17116/anaesthesiology201903143

[6] Попугаев К.А., Солодов А.А., Суряхин В.С., и др. Управление температурой в интенсивной терапии: актуальные вопросы // Анестезиология и реаниматология. 2019. № 3. С. 45–55. doi: 10.17116/anaesthesiology201903143

[7] Arthur RH. Therapeutic hypothermia: Is there still a place? Metabolic effects. In: 34th International Symposium on Intensive Care and Emergency Medicine. Brussels; 2014.

[8] Arthur R.H. Therapeutic hypothermia: Is there still a place? Metabolic effects // 34th International Symposium on Intensive Care and Emergency Medicine. Brussels, Belgium, 18–21 March 2014. Brussels, 2014.

[9] Shevelev OA, Butrov AV, Cheboksary DV, et al. Pathogenetic role of cerebral hyperthermia in brain lesions. Clin Med. 2017;95(4):302–309. (In Russ). doi: 10.18821/0023-2149-2017-95-4-302-309 309

[10] Шевелев О.А., Бутров А.В., Чебоксаров Д.В., и др. Патогенетическая роль церебральной гипертермии при поражении головного мозга // Клиническая медицина. 2017. Т. 95, № 4. С. 302–309. doi: 10.18821/0023-2149-2017-95-4-302-309

[11] Shevelev OA, Saidov ShKh, Petrova MV, et al. Craniocerebral hypothermia as a method of therapy of disorders of the temperature balance of the brain in patients in the postcomatous period. Physical and Rehabilitation Medicine, Medical Rehabilitation. 2019;19(4):56–63. (In Russ). doi: 10.36425/2658-6843-2019-4-56-63

[12] Шевелев О.А., Саидов Ш.Х., Петрова М.В., и др. Коррекция нарушений теплового баланса головного мозга в терапии и реабилитации пациентов с церебральной патологией // Физическая и реабилитационная медицина, медицинская реабилитация. 2019. Т. 1, № 4. С. 56–63. doi: 10.36425/2658-6843-2019-4-56-63

[13] Torosyan BD, Butrov AV, Shevelev OA, et al. The effect of craniocerebral hypothermia on oxygen consumption, basal metabolism and central hemodynamic parameters in patients in the acute period of ischemic stroke. Medical Alphabet. 2017;2(17):26–29. (In Russ).

[14] Торосян Б.Д., Бутров А.В., Шевелев О.А., и др. Влияние краниоцеребральной гипотермии на потребление кислорода, основной обмен и показатели центральной гемодинамики у пациентов в остром периоде ишемического инсульта // Медицинский алфавит. 2017. Т. 2, № 17. С. 26–29.

[15] Shevelev OA, Petrova MV, Saidov ShKh, et al. Mechanisms of neuroprotection in cerebral hypothermia (review). General Resuscitation. 2019;15(6):94–114. (In Russ). doi: 10.15360/1813-9779-2019-6-94-114

[16] Шевелев О.А., Петрова М.В., Саидов Ш.Х., и др. Механизмы нейропротекции при церебральной гипотермии (обзор) // Общая реаниматология. 2019. Т. 15, № 6. С. 94–114. doi: 10.15360/1813-9779-2019-6-94-114

[17] Giacino JT, Fins JJ, Laureys S, et al. Disorders of consciousness after acquired brain injury: the state of the science. Nat Rev Neurol. 2014;10(2):99–114. doi: 10.1038/nrneurol.2013.279

[18] Giacino J.T., Fins J.J., Laureys S., et al. Disorders of consciousness after acquired brain injury: the state of the science // Nature Reviews Neurology. 2014. Vol. 10, N 2. Р. 99–114. doi: 10.1038/nrneurol.2013.279

[19] Piradov MV, Suponeva NA, Sergeev DV, et al. Structural and functional foundations of chronic disorders of consciousness. Ann Clin Exp Neurol. 2018;12(Suppl. 5):6–15. (In Russ). doi: 10.25692/ACEN.2018.5.1

[20] Пирадов М.В., Супонева Н.А., Сергеев Д.В., и др. Структурно-функциональные основы хронических нарушений сознания // Анналы клинической и экспериментальной неврологии. 2018. Т. 12, № 5S. С. 6–15. doi: 10.25692/ACEN.2018.5.1

[21] Petrova MV, Shevelev OA, Saidov ShKh, Mohan R. Features of the thermal balance of the brain in patients in a chronic critical condition. In: 39th International Symposium on Intensive Care and Emergency Medicine. Brussels, Belgium, March 19–22, 2019. Brussels; 2019. P. 215. (In Russ). doi: 10.1186/s13054-019-2358-0

[22] Petrova M.V., Shevelev O.A., Saidov Sh.Kh., Mohan R. Features of the thermal balance of the brain in patients in a chronic critical condition // 39th International Symposium on Intensive Care and Emergency Medicine. Brussels, Belgium, March 19–22, 2019. Brussels, 2019. Р. 215. doi: 10.1186/s13054-019-2358-0

[23] Mrozek S, Vardon F., Geeraerts T. Brain temperature: physiology and pathophysiology after brain injury. Anesthesiol Res Pract. 2012:989487. doi: 10.1155/2012/989487

[24] Mrozek S., Vardon F., Geeraerts T. Brain temperature: physiology and pathophysiology after brain injury // Anesthesiol Res Pract. 2012. Р. 989487. doi: 10.1155/2012/989487

[25] Ribeiro PF, Ventura-Antunes RL, Gabi M, еt al. The human cerebral cortex is neither one nor many: neuronal distribution reveals two quantitatively different zones in the gray matter, three in the white matter, and explains local variations in cortical folding. Front Neuroanat. 2013;7:28. doi: 10.3389/fnana.2013.00028

[26] Ribeiro P.F., Ventura-Antunes R.L., Gabi M., еt al. The human cerebral cortex is neither one nor many: neuronal distribution reveals two quantitatively different zones in the gray matter, three in the white matter, and explains local variations in cortical folding // Front Neuroanat. 2013. Vol. 7. Р. 28. doi: 10.3389/fnana.2013.00028

[27] Torosyan BD, Burov AV, Shevelev OA, et al. The effect of craniocerebral hypothermia on metabolism in patients in the acute period of ischemic stroke. Medical Alphabet. 2018;1(9):41–44. (In Russ).

[28] Торосян Б.Д., Бутров А.В., Шевелев О.А., и др. Влияние кранио церебральной гипотермии на метаболизм у пациентов в остром периоде ишемического инсульта // Медицинский алфавит. 2018. Т. 1, № 9. С. 41–44.

[29] Kiyatkin ЕА. Brain temperature: from physiology and pharmacology to neuropathology. In: Romanovsky AA, editor. Handbook of Clinical Neurology. Vol. 157: Thermoregulation: From Basic Neuroscience to Clinical Neurology, Part II. Elsevier, 2018. Р. 483–504. doi: 10.1016/B978-0-444-64074-1.00030-6

[30] Kiyatkin Е.А. Brain temperature: from physiology and pharmacology to neuropathology // Romanovsky A.A., editor. Handbook of Clinical Neurology. Vol. 157: Thermoregulation: From Basic Neuroscience to Clinical Neurology, Part II. Elsevier, 2018. Р. 483–504. doi: 10.1016/B978-0-444-64074-1.00030-6

[31] Childs C, Yrjö H, Vidyasagar R, Kauppinen R. Determination of regional brain temperature using proton magnetic resonance spectroscopy to assess brain-body temperature differences in healthy human subjects. Magnetic Res Med. 2007;57(1):59–66. doi: 10.1002/mrm.21100

[32] Childs C., Yrjö H., Vidyasagar R., Kauppinen R. Determination of regional brain temperature using proton magnetic resonance spectroscopy to assess brain-body temperature differences in healthy human subjects // Magnetic Res Med. 2007. Vol. 57, N 1. Р. 59–66. doi: 10.1002/mrm.21100

RIGHTS & PERMISSIONS

Petrova M.V., Mengistu E.M., Shevelev O.A., Kostenkova I.Z., Yuriev M.Y., Zhdanova M.A.