Anesthesia-Induced Oxidative Stress: Are There Differences between Intravenous and Inhaled Anesthetics?

Thomas Senoner, Corinna Velik-Salchner, Günter Luckner, Helmuth Tauber, Thomas Senoner, Corinna Velik-Salchner, Günter Luckner, Helmuth Tauber

Abstract

Agents used for the induction of anesthesia have been shown to either promote or mitigate oxidative stress. A fine balance between the presence of reactive oxygen species (ROS) and antioxidants is crucial for the proper normal functioning of the cell. A basal concentration of ROS is essential for the manifestation of cellular functions, whereas disproportionate levels of ROS cause damage to cellular macromolecules such as DNA, lipids, and proteins, eventually leading to necrosis and apoptosis. Increased ROS has been linked with numerous illnesses, such as cardiovascular, immune system, liver, and kidney, and has been shown to promote cancer and accelerate aging. Knowledge of the various pharmacologic agents that increase or reduce oxidative stress may promote a safer way of inducing anesthesia. Furthermore, surgery itself leads to increased ROS production and ischemia/reperfusion injury. Indeed, increased perioperative oxidative stress has been correlated with increased postoperative complications and prolonged recovery. Anesthesiologists care for patients during the whole spectrum of perioperative care and thus are in a unique position to deliver countermeasures to oxidative stress. Using preferentially an induction agent which reduces oxidative stress might lead to better clinical outcomes and fewer postoperative complications. Propofol has been shown in several studies to reduce oxidative stress, which reduces postoperative complications and leads to a faster recovery, and thus might represent the preferred induction agent in the right clinical setting.

Conflict of interest statement

The authors declare that there is no conflict of interest.

Copyright © 2021 Thomas Senoner et al.

Figures

Figure 1
Figure 1
Chemical structures of the inhaled anesthetics discussed in this paper.
Figure 2
Figure 2
Chemical structures of the intravenous anesthetics discussed in this paper.

References

    1. Hussain S. P., Hofseth L. J., Harris C. C. Radical causes of cancer. Nature Reviews Cancer . 2003;3(4):276–285. doi: 10.1038/nrc1046.
    1. Sanders L. H., Greenamyren J. T. Oxidative damage to macromolecules in human Parkinson disease and the rotenone model. Free Radical Biology and Medicine . 2013;62:111–120. doi: 10.1016/j.freeradbiomed.2013.01.003.
    1. Song B. C., Joo N. S., Aldini G., Yeum K. J. Biological functions of histidine-dipeptides and metabolic syndrome. Nutrition Research and Practice . 2014;8(1):3–10. doi: 10.4162/nrp.2014.8.1.3.
    1. Senoner T., Dichtl W. Oxidative stress in cardiovascular diseases: still a therapeutic target? Nutrients . 2019;11(9):p. 2090. doi: 10.3390/nu11092090.
    1. Liochev S. I. Reactive oxygen species and the free radical theory of aging. Free Radical Biology & Medicine . 2013;60:1–4. doi: 10.1016/j.freeradbiomed.2013.02.011.
    1. Holmström K. M., Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nature Reviews. Molecular Cell Biology . 2014;15(6):411–421. doi: 10.1038/nrm3801.
    1. Finkel T. Signal transduction by reactive oxygen species. The Journal of Cell Biology . 2011;194(1):7–15. doi: 10.1083/jcb.201102095.
    1. Balaban R. S., Nemoto S., Finkel T. Mitochondria, oxidants, and aging. Cell . 2005;120(4):483–495. doi: 10.1016/j.cell.2005.02.001.
    1. Omling E., Jarnheimer A., Rose J., Björk J., Meara J. G., Hagander L. Population-based incidence rate of inpatient and outpatient surgical procedures in a high-income country. The British Journal of Surgery . 2018;105(1):86–95. doi: 10.1002/bjs.10643.
    1. Senoner T., Schindler S., Stättner S., Öfner D., Troppmair J., Primavesi F. Associations of oxidative stress and postoperative outcome in liver surgery with an outlook to future potential therapeutic options. Oxidative Medicine and Cellular Longevity . 2019;2019:18. doi: 10.1155/2019/3950818.
    1. Arsalani-Zadeh R., Ullah S., Khan S., MacFie J. Oxidative Stress in Laparoscopic _Versus_ Open Abdominal Surgery: A Systematic Review. Journal of Surgical Research . 2011;169(1):e59–e68. doi: 10.1016/j.jss.2011.01.038.
    1. Tsuchiya M., Shiomoto K., Mizutani K., et al. Reduction of oxidative stress a key for enhanced postoperative recovery with fewer complications in esophageal surgery patients. Medicine . 2018;97(47):p. e12845. doi: 10.1097/MD.0000000000012845.
    1. Plicner D., Mazur P., Sadowski J., Undas A. Asymmetric dimethylarginine and oxidative stress following coronary artery bypass grafting: associations with postoperative outcome. European Journal of Cardio-Thoracic Surgery . 2014;45(5):e136–e141. doi: 10.1093/ejcts/ezt646.
    1. Hsu J.-C., Huang C.-Y., Chuang S.-L., et al. Long term outcome of postoperative atrial fibrillation after cardiac surgery-a propensity score-matched cohort analysis. Frontiers in Cardiovascular Medicine . 2021;8 doi: 10.3389/fcvm.2021.650147.
    1. Wu J. H. Y., Marchioli R., Silletta M. G., et al. Oxidative stress biomarkers and incidence of postoperative atrial fibrillation in the omega-3 fatty acids for prevention of postoperative atrial fibrillation (OPERA) trial. Journal of the American Heart Association . 2015;4(5) doi: 10.1161/JAHA.115.001886.
    1. Whalen F. X., Bacon D. R., Smith H. M. Inhaled anesthetics: an historical overview. Best Practice and Research: Clinical Anaesthesiology . 2005;19(3):323–330. doi: 10.1016/j.bpa.2005.02.001.
    1. Eger E. I., Raines D. E., Shafer S. L., Hemmings H. C., Sonner J. M. Is a new paradigm needed to explain how inhaled anesthetics produce immobility? Anesthesia and Analgesia . 2008;107(3):832–848. doi: 10.1213/ane.0b013e318182aedb.
    1. Hemmings H. C., Akabas M. H., Goldstein P. A., Trudell J. R., Orser B. A., Harrison N. L. Emerging molecular mechanisms of general anesthetic action. Trends in Pharmacological Sciences . 2005;26(10):503–510. doi: 10.1016/j.tips.2005.08.006.
    1. Sonner J. M., Antognini J. F., Dutton R. C., et al. Inhaled anesthetics and immobility: mechanisms, mysteries, and minimum alveolar anesthetic concentration. Anesthesia and Analgesia . 2003;97(3):718–740. doi: 10.1213/01.ANE.0000081063.76651.33.
    1. Juhász M., Molnár L., Fülesdi B., Végh T., Páll D., Molnár C. Effect of sevoflurane on systemic and cerebral circulation, cerebral autoregulation and CO2 reactivity. BMC Anesthesiology . 2019;19(1):p. 109. doi: 10.1186/s12871-019-0784-9.
    1. Holmström A., Åkeson J. Sevoflurane induces less cerebral vasodilation than isoflurane at the same A-line® autoregressive index level. Acta Anaesthesiologica Scandinavica . 2005;49(1):16–22. doi: 10.1111/j.1399-6576.2004.00576.x.
    1. Qin Y., Ni J., Kang L., Zhong Z., Wang L., Yin S. Sevoflurane effect on cognitive function and the expression of oxidative stress response proteins in elderly patients undergoing radical surgery for lung cancer. Journal of the College of Physicians and Surgeons Pakistan . 2019;29(1):12–15. doi: 10.29271/jcpsp.2019.01.12.
    1. Herrmann M., Vos P., Wunderlich M. T., De Bruijn C. H. M. M., Lamers K. J. B. Release of glial tissue-specific proteins after acute stroke: a comparative analysis of serum concentrations of protein S-100B and glial fibrillary acidic protein. Stroke . 2000;31(11):2670–2677. doi: 10.1161/01.STR.31.11.2670.
    1. Cukurova Z., Cetingok H., Ozturk S., et al. DNA damage effects of inhalation anesthetics in human bronchoalveolar cells. Medicine . 2019;98(32):p. e16518. doi: 10.1097/MD.0000000000016518.
    1. Valavanidis A., Vlachogianni T., Fiotakis C. 8-Hydroxy-2’ -deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. Journal of Environmental Science and Health, Part C . 2009;27(2):120–139. doi: 10.1080/10590500902885684.
    1. Sanchez V., Feinstein S. . D., Lunardi N., et al. General anesthesia causes long-term impairment of mitochondrial morphogenesis and synaptic transmission in developing rat brain. Anesthesiology . 2011;115(5):992–1002. doi: 10.1097/ALN.0b013e3182303a63.
    1. Jevtovic-Todorovic V., Hartman R. E., Izumi Y., et al. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. The Journal of Neuroscience . 2003;23(3):876–882. doi: 10.1523/JNEUROSCI.23-03-00876.2003.
    1. Jevtovic-Todorovic V., Absalom A. R., Blomgren K., et al. Anaesthetic neurotoxicity and neuroplasticity: an expert group report and statement based on the BJA Salzburg Seminar. British Journal of Anaesthesia . 2013;111(2):143–151. doi: 10.1093/bja/aet177.
    1. Davidson A. J., Disma N., de Graaff J. C., et al. Neurodevelopmental outcome at 2 years of age after general anaesthesia and awake-regional anaesthesia in infancy (GAS): an international multicentre, randomised controlled trial. Lancet . 2016;387(10015):239–250. doi: 10.1016/S0140-6736(15)00608-X.
    1. Ebert T. J., Perez F., Uhrich T. D., Deshur M. A. Desflurane-mediated sympathetic activation occurs in humans despite preventing hypotension and baroreceptor unloading. Anesthesiology . 1998;88(5):1227–1232. doi: 10.1097/00000542-199805000-00013.
    1. Cinnella G., Vendemiale G., Dambrosio M., et al. Effect of propofol, sevoflurane and desflurane on systemic redox balance. International Journal of Immunopathology and Pharmacology . 2007;20(3):585–593. doi: 10.1177/039463200702000316.
    1. Nogueira F. R., Braz L. G., de Andrade L. R., et al. Evaluation of genotoxicity of general anesthesia maintained with desflurane in patients under minor surgery. Environmental and Molecular Mutagenesis . 2016;57(4):312–316. doi: 10.1002/em.22012.
    1. Nogueira F. R., Braz L. G., Souza K. M., et al. Comparison of DNA damage and oxidative stress in patients anesthetized with desflurane associated or not with nitrous oxide: a prospective randomized clinical trial. Anesthesia and Analgesia . 2018;126(4):1198–1205. doi: 10.1213/ANE.0000000000002729.
    1. Eroglu F., Yavuz L., Ceylan B. G., et al. New volatile anesthetic, desflurane, reduces vitamin e level in blood of operative patients via oxidative stress. Cell Biochemistry and Function . 2010;28(3):211–216. doi: 10.1002/cbf.1641.
    1. Yalcin S., Aydoğan H., Yuce H. H., et al. Effects of sevoflurane and desflurane on oxidative stress during general anesthesia for elective cesarean section. Wiener Klinische Wochenschrift . 2013;125(15–16):467–473. doi: 10.1007/s00508-013-0397-0.
    1. Ball C., Westhorpe R. N. Isoflurane. Anaesthesia and Intensive Care . 2007;35(4):p. 467. doi: 10.1177/0310057X0703500401.
    1. Wei H., Kang B., Wei W., et al. Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Research . 2005;1037(1–2):139–147. doi: 10.1016/j.brainres.2005.01.009.
    1. Xie Z., Dong Y., Maeda U., et al. The common inhalation anesthetic isoflurane induces apoptosis and increases amyloid β protein levels. Anesthesiology . 2006;104(5):988–994. doi: 10.1097/00000542-200605000-00015.
    1. Eckenhoff R. G., Johansson J. S., Wei H., et al. Inhaled anesthetic enhancement of amyloid-β oligomerization and cytotoxicity. Anesthesiology . 2004;101(3):703–709. doi: 10.1097/00000542-200409000-00019.
    1. Callaway J. K., Jones N. C., Royse C. F. Isoflurane induces cognitive deficits in the Morris water maze task in rats. European Journal of Anaesthesiology . 2012;29(5):239–245. doi: 10.1097/EJA.0b013e32835103c1.
    1. Culley D. J., Baxter M., Yukhananov R., Crosby G. The memory effects of general anesthesia persist for weeks in young and aged rats. Anesthesia and Analgesia . 2003;96(4):1004–1009. doi: 10.1213/01.ANE.0000052712.67573.12.
    1. Bianchi S. L., Tran T., Liu C. L., et al. Brain and behavior changes in 12-month-old Tg2576 and nontransgenic mice exposed to anesthetics. Neurobiology of Aging . 2008;29(7):1002–1010. doi: 10.1016/j.neurobiolaging.2007.02.009.
    1. Ni C., Li C., Dong Y., Guo X., Zhang Y., Xie Z. Anesthetic isoflurane induces DNA damage through oxidative stress and p53 pathway. Molecular Neurobiology . 2017;54(5):3591–3605. doi: 10.1007/s12035-016-9937-8.
    1. Braz M. G., Braz L. G., Freire C. M. M., et al. Isoflurane and propofol contribute to increasing the antioxidant status of patients during minor elective surgery: a randomized clinical study. Medicine (Baltimore) . 2015;94(31):p. e1266. doi: 10.1097/MD.0000000000001266.
    1. Lew V., McKay E., Maze M. Past, present, and future of nitrous oxide. British Medical Bulletin . 2018;125(1):103–119. doi: 10.1093/bmb/ldx050.
    1. Yamakura T., Harris R. A. Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels: comparison with isoflurane and ethanol. Anesthesiology . 2000;93(4):1095–1101. doi: 10.1097/00000542-200010000-00034.
    1. Hendrickx J., Peyton P., Carette R., De Wolf A. Inhaled anaesthetics and nitrous oxide. European Journal of Anaesthesiology . 2016;33(9):611–619. doi: 10.1097/EJA.0000000000000467.
    1. Sawamura S., Obara M., Takeda K., Maze M., Hanaoka K. Corticotropin-releasing factor mediates the antinociceptive action of nitrous oxide in rats. Anesthesiology . 2003;99(3):708–715. doi: 10.1097/00000542-200309000-00028.
    1. Hert S. G. D. The current place of nitrous oxide in clinical practice. European Journal of Anaesthesiology . 2015;32(8):517–520. doi: 10.1097/EJA.0000000000000264.
    1. Myles P. S., Leslie K., Chan M. T. V., et al. Avoidance of nitrous oxide for patients undergoing major surgery: a randomized controlled trial. Anesthesiology . 2007;107(2):221–231. doi: 10.1097/01.anes.0000270723.30772.da.
    1. Şardaş S., Cuhruk H., Karakaya A. E., Atakurt Y. Sister-chromatid exchanges in operating room personnel. Mutation Research/Genetic Toxicology . 1992;279(2):117–120. doi: 10.1016/0165-1218(92)90253-V.
    1. Karelová J., Jablonická A., Gavora J., Hanoi Ł. Chromosome and sister-chromatid exchange analysis in peripheral lymphocytes, and mutagenicity of urine in anesthesiology personnel. International Archives of Occupational and Environmental Health . 1992;64(4):303–306. doi: 10.1007/BF00378289.
    1. Reitz M., Coen R., Lanz E. DNA single-strand breaks in peripheral lymphocytes of clinical personnel with occupational exposure to volatile inhalational anesthetics. Environmental Research . 1994;65(1):12–21. doi: 10.1006/enrs.1994.1018.
    1. Chang W. P., Lee S. R., Tu J., Hseu S. S. Increased micronucleus formation in nurses with occupational nitrous oxide exposure in operating theaters. Environmental and Molecular Mutagenesis . 1996;27(2):93–97. doi: 10.1002/(SICI)1098-2280(1996)27:2<93::AID-EM3>;2-F.
    1. Thomas P., Fenech M. Cytokinesis-block micronucleus cytome assay in lymphocytes. Methods in Molecular Biology . 2011;682:217–234. doi: 10.1007/978-1-60327-409-8_16.
    1. Jarman R. History of intravenous anaesthesia with ten years’ experience in the use of pentothal sodium. Postgraduate Medical Journal . 1946;22(252):311–318. doi: 10.1136/pgmj.22.252.311.
    1. Ruesch D., Neumann E., Wulf H., Forman S. A. An allosteric coagonist model for propofol effects on α1β2γ2L γ-aminobutyric acid type A receptors. Anesthesiology . 2012;116(1):47–55. doi: 10.1097/ALN.0b013e31823d0c36.
    1. Krasowski M. D., Koltchine V. V., Rick C. E., Ye Q., Finn S. E., Harrison N. L. Propofol and other intravenous anesthetics have sites of action on the Γ-aminobutyric acid type A receptor distinct from that for isoflurane. Molecular Pharmacology . 1998;53(3):530–538. doi: 10.1124/mol.53.3.530.
    1. Kushikata T., Hirota K., Yoshida H., Kubota T., Ishihara H., Matsuki A. Alpha-2 adrenoceptor activity affects propofol-induced sleep time. Anesthesia and Analgesia . 2002;94(5):1201–1206. doi: 10.1097/00000539-200205000-00028.
    1. Kang M. Y., Tsuchiya M., Packer L., Manabe M. In vitro study on antioxidant potential of various drugs used in the perioperative period. Acta Anaesthesiologica Scandinavica . 1998;42(1):4–12. doi: 10.1111/j.1399-6576.1998.tb05073.x.
    1. Tsuchiya M., Asada A., Kasahara E., Sato E. F., Shindo M., Inoue M. Antioxidant protection of propofol and its recycling in erythrocyte membranes. American Journal of Respiratory and Critical Care Medicine . 2002;165(1):54–60. doi: 10.1164/ajrccm.165.1.2010134.
    1. Zhang Y., Zuo Y., Li B., et al. Propofol prevents oxidative stress and apoptosis by regulating iron homeostasis and targeting JAK/STAT3 signaling in SH-SY5Y cells. Brain Research Bulletin . 2019;153:191–201. doi: 10.1016/j.brainresbull.2019.08.018.
    1. Zorova L. D., Popkov V. A., Plotnikov E. Y., et al. Mitochondrial membrane potential. Analytical Biochemistry . 2018;552:50–59. doi: 10.1016/j.ab.2017.07.009.
    1. Han L., Zhuo Q., Zhou Y., Qian Y. Propofol protects human cardiac cells against chemical hypoxiainduced injury by regulating the JNK signaling pathways. Experimental and Therapeutic Medicine . 2020;19(3) doi: 10.3892/etm.2020.8440.
    1. Di Guo Y. L., Wang H., Wang X., et al. Propofol post-conditioning after temporary clipping reverses oxidative stress in aneurysm surgery. The International Journal of Neuroscience . 2019;129(2):155–164. doi: 10.1080/00207454.2018.1483920.
    1. Domino E. F. Taming the ketamine tiger. Anesthesiology . 2010;113(3):678–684. doi: 10.1097/ALN.0b013e3181ed09a2.
    1. Anis N. A., Berry S. C., Burton N. R., Lodge D. The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methyl-aspartate. British Journal of Pharmacology . 1983;79(2):565–575. doi: 10.1111/j.1476-5381.1983.tb11031.x.
    1. South S. M. A conditional deletion of the NR1 subunit of the NMDA receptor in adult spinal cord dorsal horn reduces NMDA currents and injury-induced pain. The Journal of Neuroscience . 2003;23(12):5031–5040. doi: 10.1523/JNEUROSCI.23-12-05031.2003.
    1. Udesky J. O., Spence N. Z., Achiel R., Lee C., Flood P. The role of nicotinic inhibition in ketamine-induced behavior. Anesthesia and Analgesia . 2005;101(2):407–411. doi: 10.1213/01.ANE.0000155291.81338.90.
    1. Hirota K., Okawa H., Appadu B. L., Grandy D. K., Devi L. A., Lambert D. G. Stereoselective interaction of ketamine with recombinant [micro sign], [small kappa, Greek], and [small delta, Greek] opioid receptors expressed in Chinese hamster ovary cells. Anesthesiology . 1999;90(1):174–182. doi: 10.1097/00000542-199901000-00023.
    1. Gelissen H. P. M. M., Epema A. H., Henning R. H., Krijnen H. J., Hennis P. J., Den Hertog A. Inotropic effects of propofol, thiopental, midazolam, etomidate, and ketamine on isolated human atrial muscle. Anesthesiology . 1996;84(2):397–403.. doi: 10.1097/00000542-199602000-00019.
    1. Khoshraftar E., Ranjbar A., Kharkhane B., Heidary S., Gharebaghi Z., Zadkhosh N. Antioxidative effects of propofol vs. ketamin in individuals undergoing surgery. Archives of Iranian Medicine . 2014;17(7):468–489.
    1. Liu H., Dai T., Yao S. Effect of thiopental sodium on N-methyl-D-aspartate-gated currents. Canadian Journal of Anesthesia . 2006;53(5):442–448. doi: 10.1007/BF03022615.
    1. Judge S. E. Effect of general anaesthetics on synaptic ion channels. British Journal of Anaesthesia . 1983;55(3):191–200. doi: 10.1093/bja/55.3.191.
    1. Tomlin S. L., Jenkins A., Lieb W. R., Franks N. P. Preparation of barbiturate optical isomers and their effects on GABA(A) receptors. Anesthesiology . 1999;90(6):1714–1722.. doi: 10.1097/00000542-199906000-00029.
    1. Liu H., Yao S. Thiopental sodium reduces glutamate extracellular levels in rat intact prefrontal cortex. Experimental Brain Research . 2005;167(4):666–669. doi: 10.1007/s00221-005-0243-3.
    1. Wilson J. X., Gelb A. W. Free radicals, antioxidants, and neurologic injury: possible relationship to cerebral protection by anesthetics. Journal of Neurosurgical Anesthesiology . 2002;14(1):66–79. doi: 10.1097/00008506-200201000-00014.
    1. Winsky-Sommerer R. Role of GABAAreceptors in the physiology and pharmacology of sleep. European Journal of Neuroscience . 2009;29(9):1779–1794. doi: 10.1111/j.1460-9568.2009.06716.x.
    1. Reynolds L. M., Engin E., Tantillo G., et al. Differential Roles of GABAA Receptor Subtypes in Benzodiazepine-Induced Enhancement of Brain-Stimulation Reward. Neuropsychopharmacology . 2012;37(11):2531–2540. doi: 10.1038/npp.2012.115.
    1. Möhler H., Fritschy J. M., Rudolph U. A new benzodiazepine pharmacology. Journal of Pharmacology and Experimental Therapeutics . 2002;300(1):2–8. doi: 10.1124/jpet.300.1.2.
    1. Saari T. I., Uusi-Oukari M., Ahonen J., Olkkola K. T. Enhancement of GABAergic activity: neuropharmacological effects of benzodiazepines and therapeutic use in anesthesiology. Pharmacological Reviews . 2011;63(1):243–267. doi: 10.1124/pr.110.002717.
    1. Xia W. F., Liu Y., Zhou Q. S., Tang Q. Z., Zou H. D. Comparison of the effects of propofol and midazolam on inflammation and oxidase stress in children with congenital heart disease undergoing cardiac surgery. Yonsei Medical Journal . 2011;52(2):326–332. doi: 10.3349/ymj.2011.52.2.326.

Source: PubMed

3
購読する