350 rub
Journal Biomedical Radioelectronics №2-3 for 2022 г.
Article in number:
Analysis of modern ideas about the inert gases neuroprotective properties
Type of article: overview article
DOI: https://doi.org/10.18127/j15604136-202202-05
UDC: 615.835.56
Authors:

L.Yu. Marchenko1, E.E. Sigaleva2, E.I. Matsnev3, V.V. Pyatenko4

1–4 State Scientific Center of the Russian Federation Institute for Biomedical Problems of the RAS (Moscow, Russia)

Abstract:

In accordance with modern concepts, hypoxic-ischemic and inflammatory processes form the pathogenetic basis of central and peripheral nervous system diseases. Taking into account the urgent task of searching for new neuroprotective strategies, the use of inert gases with proven antihypoxic and anti-inflammatory effects can become an affordable, non-invasive and safe way to protect nervous tissue from damage.

Based on the analysis of literature data on the biological properties of inert gases, substantiate the possibility of using argon, helium and krypton as promising neuroprotection means.

An analysis of modern studies devoted to research of the mechanisms of the inert gases neuroprotective action has been carried out, and the prospects for the clinical use of argon, helium and krypton in medical practice have been substantiated.

The analyzed data allow us to recommend the widespread use of oxygen and inert gases argon and helium inhalations in clinical studies to assess the neuroprotective properties of these gases in humans, as well as further study of the krypton biological effect in various experimental models.

Pages: 46-57
For citation

Marchenko L.Yu., Sigaleva E.E., Matsnev E.I., Pyatenko V.V. Analysis of modern ideas about the inert gases neuroprotective properties. Biomedicine Radioengineering. 2022. V. 25. № 2–3. Р. 46-57. DOI: https://doi.org/10.18127/j15604136-202202-05 (In Russian)

References
  1. Begun D.N., Morozova T.A., Surikova A.V. Bolezni nervnoy sistemy kak mediko-sotsialnaya problema. Molodoy uchenyy. 2019. T. 248. № 10. S. 78–80. (in Russian).
  2. Isaykin A.I., Chernyshova E.A., Yakhno N.N. Primeneniye neyroprotektivnoy terapii pri insultakh i cherepno-mozgovoy travme. Trudnyy patsiyent. 2012. T. 10. № 11. S. 18–21. (in Russian).
  3. Gusev E.I., Skvortsova V.I. Neyroprotektivnaya terapiya ishemicheskogo insulta. Atmosfera. 2002. № 1. S. 3–7. (in Russian).
  4. Batysheva T.T., Boyko A.N., Kostenko E.V., Bagir L.V. Neyroprotektivnaya terapiya v nevrologicheskoy praktike. Rossiyskiy meditsinskiy zhurnal. 2007. № 10. S. 821. (in Russian).
  5. Cherniy V.I., Andronova I.A., Cherniy T.V., Gorodnik G.A. Strategiya dvukhetapnoy neyroprotektsii pri cherepno-mozgovoy travme i tserebralnom ishemicheskom insulte. Meditsina neotlozhnykh sostoyaniy. 2012. № 7–8. (46–47). S. 127–132. (in Russian).
  6. Gardner A.J., Menon D.K. Moving to human trials for argon neuroprotection in neurological injury: a narrative review. Br. J. Anaesth. 2018. V. 120. № 3. P. 453–468.
  7. Berganza C.J., John H.Z. The role of helium gas in medicine. Med. Gas. Res. 2013. V. 3. № 18. P. 2–7.
  8. Kussmaul A.R. Biologicheskoye deystviye kriptona na zhivotnykh i cheloveka v usloviyakh povyshennogo davleniya: Avtoref. dis. … kand. med. nauk. M. 2007. 23 s.
  9. Höllig A., Schug A., Fahlenkamp A.V., Rossaint R., Coburn M. Argon: Systematic Review on Neuro- and Organoprotective Properties of an “Inert” Gas. Int. J. Mol. Sci. 2014. V. 15. № 10. P. 18175–18196.
  10. Fowler B., Ackles K.N. Narcotic effects in man of breathing 80–20 argon-oxygen and air under hyperbaric conditions. Aerosp. Med. 1972. V. 43. P. 1219–1224.
  11. Bennett P.B. Prevention in rats of narcosis produced by inert gases at high pressures. Am. J. Physiol. 1963. V. 205. P. 1013–1018.
  12. Soldatov P.E., Diachenko A.I., Pavlov B.N., Fedotov A.P., Chuguyev A.P. Vyzhivayemost laboratornykh zhivotnykh v argon-soderzhashchikh gipoksicheskikh sredakh. Aviakosmicheskaya i ekologicheskaya meditsina. 1998. T. 32. №4. S. 33–37. (in Russian).
  13. Shulagin Yu.A., Diachenko A.I., Pavlov B.N. Gazoobmen cheloveka pri fizicheskoy nagruzke s ispolzovaniyem dlya dykhaniya i gipoksicheskikh KAS i KAARS. Sb. dokladov. "Indifferentnyye gazy v vodolaznoy praktike. biologii i meditsine". M.: Izd-vo "Slovo". 2000. S. 207–214. (in Russian).
  14. Jawad N., Rizvi M., Gu J., Adeyi O., Tao G., Maze M., Ma D. Neuroprotection (and lack of neuroprotection) afforded by a series of noble gases in an in vitro model of neuronal injury. Neurosci. Lett. 2009. V. 460. P. 232–236.
  15. Lemoine S., Blanchart K., Souplis M., Lemaitre A., Legallois D., Coulbault L., Simard C., Allouche S., Abraini J.H., Hanouz J.L., Rouet R., Sallé L., Guinamard R., Manrique A. Argon Exposure Induces Postconditioning in Myocardial Ischemia-Reperfusion. J. Cardiovasc. Pharmacol. Ther. 2017. V. 22. № 6. P. 564–573.
  16. Schmitz S.M., Dohmeier H., Stoppe C., Alizai P.H., Schipper S., Neumann U.P., Coburn M., Ulmer T.F. Inhaled Argon Impedes Hepatic Regeneration after Ischemia/Reperfusion Injury in Rats. Int. J. Mol. Sci. 2020. V. 21. № 15. P. 5457–5470.
  17. De Deken J., Rex S., Lerut E., Martinet W., Monbaliu D., Pirenne J., Jochmans I. Postconditioning effects of argon or xenon on early graft function in a porcine model of kidney autotransplantation. Br. J. Surg. 2018. V. 105. P. 1051–1060.
  18. Zhao H., Mitchell S., Ciechanowicz S., et al. Argon protects against hypoxic-ischemic brain injury in neonatal rats through activation of nuclear factor (erythroid-derived2)-like 2. Oncotarget. 2016. V. 7. P. 25640–25651.
  19. Grüßer L., Blaumeiser-Debarry R., Krings M., Kremer B., Höllig A., Rossaint R., Coburn M. Argon attenuates the emergence of secondary injury after traumatic brain injury within a 2-hour incubation period compared to desflurane: an in vitro study. Med. Gas. Res. 2017. V. 7. № 2. P. 93–100.
  20. Koziakova M., Harris K., Edge J.C., Franks N.P., White I.L., Dickinson R. Noble gas neuroprotection: xenon and argon protect against hypoxiceischaemic injury in rat hippocampus in vitro via distinct mechanisms. British Journal of Anaesthesia. 2019. V. 123. № 5.
    P. 601–609.
  21. Goebel U., Scheid S., Spassov S., Schallner N., Wollborn J., Buerkle H., Ulbrich F. Argon reduces microglial activation and inflammatory cytokine expression in retinal ischemia/reperfusion injury. Neural Regen. Res. 2021. V. 16. № 1. P. 192–198.
  22. Ulbrich F., Kaufmann K., Roesslein M., et al. Argon mediates anti-apoptotic signaling and neuroprotectionvia inhibition of Toll-like receptor 2 and 4. PLoS One. 2015. V. 10. P. e0143887.
  23. David H.N., Haelewyn B., Degoulet M., Colomb Jr. D.G., Risso J.J., Abraini J.H. Ex vivo and in vivo neuroprotection induced by argon when given after an excitotoxic or ischemic insult. PLoS One. 2012. V. 7. P. e30934.
  24. Gardner A.J., Menon D.K. Moving to human trials for argon neuroprotection in neurological injury: a narrative review. British Journal of Anaesthesia. 2018. V. 120. № 3. P. 453–468.
  25. Broad K.D., Fierens I., Fleiss B., et al. Inhaled 45-50% argon augments hypothermic brain protection in a piglet model of perinatal asphyxia. Neurobiol. Dis. 2016. V. 87. P. 29–38.
  26. Ulbrich F., Lerach T., Biermann J., et al. Argon mediates protection by interleukin-8 suppression via a TLR2/TLR4/ STAT3/NF-kappaB pathway in a model of apoptosis in neuroblastoma cells in vitro and following ischemia/reperfusion injury in rat retina in vivo. J. Neurochem. 2016. V. 138. P. 859–873.
  27. Brucken A., Kurnaz P., Bleilevens C., et al. Delayed argon administration provides robust protection against cardiac arrest-induced neurological damage. Neurocrit. Care. 2015. V. 22. P. 112–120.
  28. Brücken A., Bleilevens C., Föhr P., Nolte K., Rossaint R., Gernot Marx, Fries M., Derwall M. Influence of argon on temperature modulation and neurological outcome in hypothermia treated rats following cardiac arrest. Resuscitation. 2017. V. 117. P. 32–39.
  29. Fumagalli F., Olivari D., Boccardo A., De Giorgio D., Affatato R., Ceriani S., Bariselli S., Sala G., Cucino A., Zani D., Novelli D., Babini G., Magliocca A., Ilaria R., Staszewsky L., Salio M., Lucchetti J., Maisano A.M., Fiordaliso F., Furlan R., Gobbi M., Luini M.V., Pravettoni D., Scanziani E., Belloli A., Latini R., Ristagno G. Ventilation With Argon Improves Survival With Good Neurological Recovery After Prolonged Untreated Cardiac Arrest in Pigs. J. Am. Heart Assoc. 2020. V. 9. P. e016494.
  30. Yarin Y.M., Amarjargal N., Fuchs J., Haupt H., Mazurek B., Morozova S.V., Gross J. Argon protects hypoxia-, cisplatin- and gentamycin-exposed hair cells in the newborn rat’s organ of Corti. Hear. Res. 2005. V. 201. P. 1–9.
  31. Matsnev E.I., Sigaleva E.E., Tikhonova G.A., Buravkova L.B. Otoprotektivnyy effekt argona pri vozdeystvii shuma. Vestnik otorinolaringologii. 2007. №3. S. 22–26. (in Russian).
  32. Sposob otoprotektsii pri vozdeystvii shuma na organizm cheloveka: Pat. 2376041 RF №2008116306/14. (in Russian).
  33. Sposob provedeniya spasatelnykh meropriyatiy: Pat. 2390358 RF № 2009107543/12.
  34. Abraini J.H., Kriem B., Balon N., Rostain J.C., Risso J.J. Gamma-aminobutyric acid neuropharmacological investigations on narcosis produced by nitrogen, argon, or nitrous oxide. Anesth. Analg. 2003. V. 96. P. 746–749.
  35. Harris K., Armstrong S.P., Campos-Pires R., Kiru L., Franks N.P., Dickinson R. Neuroprotection against traumatic brain injury by xenon, but not argon, is mediated by inhibition at the N-methyl-D-aspartate receptor glycine site. Anesthesiology. 2013. V. 119. P. 1137–1148.
  36. Brucken A., Kurnaz P., Bleilevens C., Derwall M., Weis J., Nolte K., Rossaint R., Fries M. Dose dependent neuroprotection of the noble gas argon after cardiac arrest in rats is not mediated by KATP-channel opening. Resuscitation. 2014. V. 85. P. 826–832.
  37. Fahlenkamp A.V., Rossaint R., Haase H., Al Kassam H., Ryang Y.M. Beyer C., Coburn M. The noble gas argon modifies extracellular signal-regulated kinase 1/2 signaling in neurons and glial cells. Eur. J. Pharmacol. 2012. V. 674. P. 104–111.
  38. Liu J., Nolte K., Brook G., Liebenstund L., Weinandy A., Höllig A., Veldeman M., Willuweit A., Karl-Josef L., Rossaint R., Coburn M. Post-stroke treatment with argon attenuated brain injury, reduced brain inflammation and enhanced M2 microglia/ macrophage polarization: a randomized controlled animal study. Critical Care. 2019. V. 23. № 1. P. 2–13.
  39. Kremer B., Coburn M., Weinandy A., Nolte K., Clusmann H., Veldeman M., Höllig A. Argon treatment after experimental subarachnoid hemorrhage: evaluation of microglial activation and neuronal survival as a subanalysis of a randomized controlled animal trial. Med. Gas. Res. 2020. V. 10. №3. P. 103–109.
  40. Moro F., Fossi F., Magliocca A., Pascente R., Sammali E., Baldini F., Tolomeo D., Micotti E., Citerio G., Stocchetti N., Fumagalli F., Magnoni S., Latini R., Ristagno G., R. Zanier E.R. Efficacy of acute administration of inhaled argon on traumatic brain injury in mice. British Journal of Anaesthesia. 2021. V. 126. № 1. P. 256–264.
  41. Liu J., Veldeman M., Höllig A., Nolte K., Liebenstund L., Willuweit A., Langen K.‑J., Rossaint R., Coburn M. Post‑stroke treatment with argon preserved neurons and attenuated microglia/macrophage activation long‑termly in a rat model of transient middle cerebral artery occlusion (tMCAO). Scientific Reports. 2022. V. 12. № 1. P. 691.
  42. Krasnovskiy A.L., Grigoryev S.P., Loshkareva E.O., Zolkina I.V. Ispolzovaniye gelioksa v lechenii bolnykh s bronkholegochnoy patologiyey. Rossiyskiy meditsinskiy zhurnal. 2012. № 5. S. 46–51. (in Russian).
  43. Shogenova L.V. Effekty primeneniya gelioksa kak rabochego gaza pri provedenii ingalyatsii ?2-agonistov pri pomoshchi nebulayzera u bolnykh s obostreniyem BA. Effektivnaya farmakoterapiya. 2010. № 27. S. 34–40. (in Russian).
  44. Pavlov B.N., Diachenko A.I., Shulagin Yu.A., Pavlov N.B., Buravkova L.B., Popova Yu.A., Manyugina O.V., Sytnik E.B. Issledovaniya fiziologicheskikh effektov dykhaniya podogretymi kislorodno-geliyevymi smesyami. Fiziologiya cheloveka. 2003. T.29. № 5. S. 69–73. (in Russian).
  45. Indinnimeo L., Chiappini E., Miraglia Del Giudice., Bernardini M.R. Guideline on management of the acute asthma attack in children by Italian Society of Pediatrics. Ital. J. Pediatr. 2018. V. 44. № 46. P. 2–10.
  46. Nawab U.S., Touch S.M., Irwin-Sherman T., Blackson T.J., Greenspan J.S., Zhu G., Shaffer T.H., Wolfson M.R. Heliox attenuates lung inflammation and structural alterations in acute lung injury. Pediatr. Pulmonol. 2005. V. 6. P. 524–532.
  47. Weber N.C., Preckel B. Gaseous mediators: an updated review onthe effects of helium beyond blowing up Balloons. Intensive Care Medicine Experimental. 2019. V. 7. № 73. P. 2–14.
  48. Smit K.F., Oei G.T.M.L., Brevoord D. et al. Helium induces preconditioning in human endothelium in vivo. Anesthesiology. 2013.
    V. 118. P. 95–104.
  49. Pagel P.S., Krolikowski J.G., Shim Y.H. et al. Noble gases without anesthetic properties protect myocardium against infarction by activating prosurvival signaling kinases and inhibiting mitochondrial permeability transition in vivo. Anesth. Analg. 2007. V. 105. P. 562– 569.
  50. Pagel P.S., Krolikowski J.G., Pratt P.F. et al. Inhibition of glycogen synthase kinase or the apoptotic protein p53 lowers the threshold of helium cardioprotection in vivo: the role of mitochondrial permeability transition. Anesth. Analg. 2008. V. 107. P. 769–775.
  51. Pagel P.S., Krolikowski J.G., Amour J. et al. Morphine reduces the threshold of helium preconditioning against myocardial infarction: the role of opioid receptors in rabbits. J. Cardiothorac. Vasc. Anesth. 2009. V. 23. P. 619–624.
  52. Liu Y., Xue F., Liu G. et al. Helium preconditioning attenuates hypoxia/ischemia-induced injury in the developing brain. Brain Res. 2011. V. 1376. P. 122–129.
  53. Pan Y., Zhang H., Acharya A.B. et al. The effect of heliox treatment in a rat model of focal transient cerebral ischemia. Neurosci. Lett. 2011. V. 497. P. 144–147.
  54. Zhang R., Yu Y., Manaenko A. et al. Effect of helium preconditioning on neurological decompression sickness in rats. J. Appl. Physiol. 2019. V. 126. P. 934–940.
  55. Li Y., Liu K., Kang Z.M., Sun X.J., Liu W.W., Mao Y.F. Helium preconditioning protects against neonatal hypoxia–ischemia via nitric oxide mediated up-regulation of antioxidases in a rat model. Behavioural Brain Research. 2016. V. 300. P. 31–37.
  56. Yi Li, Peixi Zhang, Ying Liu, Wenwu Liu, Na Yin Helium preconditioning protects the brain against hypoxia/ischemia injury via improving the neurovascular niche in a neonatal rat model. Behav Brain Res. 2016. V. 314. P. 165–172.
  57. Deng Ru-Ming, Li Hai-Ying, Li Xiang, Hai-Tao Shen, De-Gang Wu, Zhong Wang, Gang Chen Neuroprotective effect of helium after neonatal hypoxic ischemia: a narrative review. Med. Gas. Res. 2021. V. 11. № 3. P. 121–123.
  58. Weber N.C., Schilling J.M., Warmbrunn M.V. et al. Helium-induced changes in circ ulating caveolin in mice suggest a novel mechanism of cardiac protection. Int. J. Mol. Sci. 2019. V. 20. № 11. P. 2640–2658.
  59. Antonov A.A., Burov N.E. Gemodinamicheskiye effekty geliyevo-kislorodnoy terapii u patsiyentov s operirovannoy koronarnoy nedostatochnostyu. Vestnik intensivnoy terapii. 2011. № 1. S 55–59. (in Russian).
  60. Oskina D.G. Eksperimentalnaya otsenka bezopasnosti primeneniya gazovoy smesi «Kripoksa 80/20». V Sb. Mediko-biologicheskiye aspekty khimicheskoy bezopasnosti. Sbornik trudov III Vseros. nauchnoy konf. molodykh uchenykh. Pod obshchey redaktsiyey A.S. Radilova. V.R. Rembovskogo. 2018. S. 171–172. (in Russian).
  61. Rizvi M., Jawad N., Li Y., Vizcaychipi M.P., Maze M., Ma D. Effect of noble gases on oxygen and glucose deprived injury in human tubular kidney cells. Exp. Biol. Med. 2010. V. 235. P. 886–891.
  62. Dickinson R., Franks N.P. Bench-to-bedside review: Molecular pharmacology and clinical use of inert gases in anesthesia and neuroprotection. Crit. Care. 2010. V. 14. № 4. P. 229–241.
Date of receipt: 16.02.2022
Approved after review: 27.02.2022
Accepted for publication: 21.03.2022