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Published in: Journal of Anesthesia 1/2024

24-09-2023 | Anesthetics | Original Article

Effects of volatile anesthetics on circadian rhythm in mice: a comparative study of sevoflurane, desflurane, and isoflurane

Authors: Sho Sugimura, Ryo Imai, Takasumi Katoh, Hiroshi Makino, Kazuya Hokamura, Tadayoshi Kurita, Yasuhito Suzuki, Yoshitaka Aoki, Tetsuro Kimura, Kazuo Umemura, Yoshiki Nakajima

Published in: Journal of Anesthesia | Issue 1/2024

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Abstract

Purpose

Volatile anesthetics affect the circadian rhythm of mammals, although the effects of different types of anesthetics are unclear. Here, we anesthetized mice using several volatile anesthetics at two different times during the day. Our objective was to compare the effects of these anesthetics on circadian rhythm.

Methods

Male adult C57BL/6 J mice were divided into eight groups (n = 8 each) based on the anesthetic (sevoflurane, desflurane, isoflurane, or no anesthesia) and anesthesia time (Zeitgeber time [ZT] 6–12 or ZT18–24). Mice were anesthetized for 6 h using a 0.5 minimum alveolar concentration (MAC) dose under constant dark conditions. The difference between the start of the active phase before and after anesthesia was measured as a phase shift. Clock genes were measured by polymerase chain reaction in suprachiasmatic nucleus (SCN) samples removed from mouse brain after anesthesia (n = 8–9 each).

Results

Phase shift after anesthesia at ZT6–12 using sevoflurane (− 0.49 h) was smaller compared with desflurane (− 1.1 h) and isoflurane (− 1.4 h) (p < 0.05). Clock mRNA (ZT6–12, p < 0.05) and Per2 mRNA (ZT18–24, p < 0.05) expression were different between the groups after anesthesia.

Conclusion

0.5 MAC sevoflurane anesthesia administered during the late inactive to early active phase has less impact on the phase shift of circadian rhythm than desflurane and isoflurane. This may be due to differences in the effects of volatile anesthetics on the expression of clock genes in the SCN, the master clock of the circadian rhythm.
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Literature
2.
go back to reference Ludin NM, Orts-Secastian A, Cheeseman JF, Chong J, Merry AF, Cuminet D, Yamazaki S, Pawley MDM, Warman GR. General anaesthesia shifts the murine circadian clock in a time-dependant fashion. Clocks Sleep. 2021;3:87–97.CrossRefPubMedPubMedCentral Ludin NM, Orts-Secastian A, Cheeseman JF, Chong J, Merry AF, Cuminet D, Yamazaki S, Pawley MDM, Warman GR. General anaesthesia shifts the murine circadian clock in a time-dependant fashion. Clocks Sleep. 2021;3:87–97.CrossRefPubMedPubMedCentral
4.
go back to reference Li N, Stanewsky R, Popay T, Warman G, Cheeseman J. The effect of general anaesthesia on circadian rhythms in behaviour and clock gene expression of drosophila melanogaster. Clocks Sleep. 2020;23(2):434–41.CrossRef Li N, Stanewsky R, Popay T, Warman G, Cheeseman J. The effect of general anaesthesia on circadian rhythms in behaviour and clock gene expression of drosophila melanogaster. Clocks Sleep. 2020;23(2):434–41.CrossRef
5.
go back to reference Kadota K, Iijima N, Hayashi Y, Takumi K, Higo S, Sakamoto A, Ozawa H. Time–dependent repression of mPer2 expression in the suprachiasmatic nucleus by inhalation anesthesia with sevoflurane. Neurosci Lett. 2012;528:153–8.CrossRefPubMed Kadota K, Iijima N, Hayashi Y, Takumi K, Higo S, Sakamoto A, Ozawa H. Time–dependent repression of mPer2 expression in the suprachiasmatic nucleus by inhalation anesthesia with sevoflurane. Neurosci Lett. 2012;528:153–8.CrossRefPubMed
6.
go back to reference Challet E, Gourmelen S, Pevet P, Oberling P, Pain L. Reciprocal relationships between general (Propofol) anesthesia and circadian time in rats. Neuropsychopharmacology. 2007;32:728–35.CrossRefPubMed Challet E, Gourmelen S, Pevet P, Oberling P, Pain L. Reciprocal relationships between general (Propofol) anesthesia and circadian time in rats. Neuropsychopharmacology. 2007;32:728–35.CrossRefPubMed
7.
go back to reference Wee BE, Turek FW. Midazolam, a short–acting benzodiazepine, resets the circadian clock of the hamster. Pharmacol Biochem Behav. 1989;32:901–6.CrossRefPubMed Wee BE, Turek FW. Midazolam, a short–acting benzodiazepine, resets the circadian clock of the hamster. Pharmacol Biochem Behav. 1989;32:901–6.CrossRefPubMed
8.
go back to reference Montaigne D, Marechal X, Modine T, Coisne A, Mouton S, Fayad G, Ninni S, Klein C, Ortmans S, Seunes C, Potelle C, Berthier A, Gheeraert C, Piveteau C, Deprez R, Eeckhoute J, Duez H, Lacroix D, Deprez B, Jegou B, Koussa M, Edme JL, Lefebvre P, Staels B. Daytime variation of perioperative myocardial injury in cardiac surgery and its prevention by Rev-Erbα antagonism: a single–centre propensity–matched cohort study and a randomised study. Lancet. 2018;391:59–69. https://doi.org/10.1016/S0140-6736(17)32132-3.CrossRefPubMed Montaigne D, Marechal X, Modine T, Coisne A, Mouton S, Fayad G, Ninni S, Klein C, Ortmans S, Seunes C, Potelle C, Berthier A, Gheeraert C, Piveteau C, Deprez R, Eeckhoute J, Duez H, Lacroix D, Deprez B, Jegou B, Koussa M, Edme JL, Lefebvre P, Staels B. Daytime variation of perioperative myocardial injury in cardiac surgery and its prevention by Rev-Erbα antagonism: a single–centre propensity–matched cohort study and a randomised study. Lancet. 2018;391:59–69. https://​doi.​org/​10.​1016/​S0140-6736(17)32132-3.CrossRefPubMed
9.
go back to reference Koike N, Yoo S, Huang H, Kumar V, Lee C, Kim T, Takahashi JS. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science. 2012;338:349–54.CrossRefPubMedPubMedCentral Koike N, Yoo S, Huang H, Kumar V, Lee C, Kim T, Takahashi JS. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science. 2012;338:349–54.CrossRefPubMedPubMedCentral
10.
go back to reference Abrahamson EE, Moore RY. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001;916:172–91.CrossRefPubMed Abrahamson EE, Moore RY. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001;916:172–91.CrossRefPubMed
12.
go back to reference Cheeseman JF, Winnebeck EC, Millar CD, Kirkland LS, Sleigh J, Goodwin M, Pawley MDM, Bloch G, Lehmann K, Menzel R, Warman GR. General anesthesia alters time perception by phase shifting the circadian clock. Proc Natl Acad Sci U S A. 2012;109:7061–6.CrossRefPubMedPubMedCentral Cheeseman JF, Winnebeck EC, Millar CD, Kirkland LS, Sleigh J, Goodwin M, Pawley MDM, Bloch G, Lehmann K, Menzel R, Warman GR. General anesthesia alters time perception by phase shifting the circadian clock. Proc Natl Acad Sci U S A. 2012;109:7061–6.CrossRefPubMedPubMedCentral
13.
go back to reference Sonner JM, Gong D, Li J, Eger EI, Laster MJ. Mouse strain modestly influences minimum alveolar anesthetic concentration and convulsivity of inhaled compounds. Anesth Analg. 1999;89:1030–4.CrossRefPubMed Sonner JM, Gong D, Li J, Eger EI, Laster MJ. Mouse strain modestly influences minimum alveolar anesthetic concentration and convulsivity of inhaled compounds. Anesth Analg. 1999;89:1030–4.CrossRefPubMed
14.
go back to reference Sato Y, Kobayashi E, Murayama T, Mishina M, Seo N. Effect of N–methyl–D–aspartate receptor epsilon1 subunit gene disruption of the action of general anesthetic drugs in mice. Anesthesiology. 2005;102:557–61.CrossRefPubMed Sato Y, Kobayashi E, Murayama T, Mishina M, Seo N. Effect of N–methyl–D–aspartate receptor epsilon1 subunit gene disruption of the action of general anesthetic drugs in mice. Anesthesiology. 2005;102:557–61.CrossRefPubMed
15.
go back to reference Quasha AL, Eger EI, Tinker TH. Determination and applications of MAC. Anesthesiology. 1980;53:315–34.CrossRefPubMed Quasha AL, Eger EI, Tinker TH. Determination and applications of MAC. Anesthesiology. 1980;53:315–34.CrossRefPubMed
16.
go back to reference Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.CrossRefPubMed Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.CrossRefPubMed
18.
go back to reference Ludin NM, Cheeseman JF, Merry AF, Millar CD, Warman GR. The effects of the general anaesthetic isoflurane on the honey bee (Apis mellifera) circadian clock. Chronobiol Int. 2016;33:128–33.CrossRefPubMed Ludin NM, Cheeseman JF, Merry AF, Millar CD, Warman GR. The effects of the general anaesthetic isoflurane on the honey bee (Apis mellifera) circadian clock. Chronobiol Int. 2016;33:128–33.CrossRefPubMed
19.
go back to reference Xia T, Cui Y, Chu S, Ma S, Gu X. Murine clock gene expression in the suprachiasmatic nuclei and peripheral blood mononuclear cells during the daily sleep–wake rhythm and after isoflurane anesthesia. Sleep Biol Rhythms. 2015;13:357–65.CrossRef Xia T, Cui Y, Chu S, Ma S, Gu X. Murine clock gene expression in the suprachiasmatic nuclei and peripheral blood mononuclear cells during the daily sleep–wake rhythm and after isoflurane anesthesia. Sleep Biol Rhythms. 2015;13:357–65.CrossRef
20.
go back to reference Xu Y, Tang P, Zhang W, Firestone L, Winter PM. Fluorine–19 nuclear magnetic resonance imaging and spectroscopy of sevoflurane uptake, distribution, and elimination in rat brain. Anesthesiology. 1995;83:766–74.CrossRefPubMed Xu Y, Tang P, Zhang W, Firestone L, Winter PM. Fluorine–19 nuclear magnetic resonance imaging and spectroscopy of sevoflurane uptake, distribution, and elimination in rat brain. Anesthesiology. 1995;83:766–74.CrossRefPubMed
21.
go back to reference Venkatasubramanian PN, Shen YJ, Wyrwicz AM. Characterization of the cerebral distribution of general anesthetics in vivo by two–dimensional 19F chemical shift imaging. Magn Reson Med. 1996;35:626–30.CrossRefPubMed Venkatasubramanian PN, Shen YJ, Wyrwicz AM. Characterization of the cerebral distribution of general anesthetics in vivo by two–dimensional 19F chemical shift imaging. Magn Reson Med. 1996;35:626–30.CrossRefPubMed
22.
go back to reference Kinjo S, Lim E, Magsaysay MV, Sands LP, Leung JM, Perioperative Medicine Research Group. Volatile anaesthetics and postoperative delirium in older surgical patients—a secondary analysis of prospective cohort studies. Acta Anaesthesiol Scand. 2019;63:18–26.CrossRefPubMed Kinjo S, Lim E, Magsaysay MV, Sands LP, Leung JM, Perioperative Medicine Research Group. Volatile anaesthetics and postoperative delirium in older surgical patients—a secondary analysis of prospective cohort studies. Acta Anaesthesiol Scand. 2019;63:18–26.CrossRefPubMed
23.
go back to reference Chen G, Zhou Y, Shi Q, Zhou H. Comparison of early recovery and cognitive function after desflurane and sevoflurane anaesthesia in elderly patients: A meta–analysis of randomized controlled trials. J Int Med Res. 2015;43:619–28.CrossRefPubMed Chen G, Zhou Y, Shi Q, Zhou H. Comparison of early recovery and cognitive function after desflurane and sevoflurane anaesthesia in elderly patients: A meta–analysis of randomized controlled trials. J Int Med Res. 2015;43:619–28.CrossRefPubMed
24.
go back to reference Rampil IJ. Anesthetic potency is not altered after hypothermic spinal cord transection in rats. Anesthesiology. 1994;80:606–10.CrossRefPubMed Rampil IJ. Anesthetic potency is not altered after hypothermic spinal cord transection in rats. Anesthesiology. 1994;80:606–10.CrossRefPubMed
25.
go back to reference Katoh T, Suguro Y, Nakajima R, Kazama T, Ikeda K. Blood concentrations of sevoflurane and isoflurane on recovery from anaesthesia. Br J Anaesth. 1992;69:259–62.CrossRefPubMed Katoh T, Suguro Y, Nakajima R, Kazama T, Ikeda K. Blood concentrations of sevoflurane and isoflurane on recovery from anaesthesia. Br J Anaesth. 1992;69:259–62.CrossRefPubMed
26.
go back to reference Dwyer R, Bennett HL, Eger EI, Heilbron D. Effects of isoflurane and nitrous oxide in subanesthetic concentrations on memory and responsiveness in volunteers. Anesthesiology. 1992;77:888–98.CrossRefPubMed Dwyer R, Bennett HL, Eger EI, Heilbron D. Effects of isoflurane and nitrous oxide in subanesthetic concentrations on memory and responsiveness in volunteers. Anesthesiology. 1992;77:888–98.CrossRefPubMed
27.
go back to reference Chortkoff BS, Eger EI 2nd, Crankshaw DP, Gonsowski CT, Dutton RC, Ionescu P. Concentrations of desflurane and propofol that suppress response to command in humans. Anesth Analg. 1995;81:737–43.PubMed Chortkoff BS, Eger EI 2nd, Crankshaw DP, Gonsowski CT, Dutton RC, Ionescu P. Concentrations of desflurane and propofol that suppress response to command in humans. Anesth Analg. 1995;81:737–43.PubMed
Metadata
Title
Effects of volatile anesthetics on circadian rhythm in mice: a comparative study of sevoflurane, desflurane, and isoflurane
Authors
Sho Sugimura
Ryo Imai
Takasumi Katoh
Hiroshi Makino
Kazuya Hokamura
Tadayoshi Kurita
Yasuhito Suzuki
Yoshitaka Aoki
Tetsuro Kimura
Kazuo Umemura
Yoshiki Nakajima
Publication date
24-09-2023
Publisher
Springer Nature Singapore
Published in
Journal of Anesthesia / Issue 1/2024
Print ISSN: 0913-8668
Electronic ISSN: 1438-8359
DOI
https://doi.org/10.1007/s00540-023-03262-9

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