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Long-Term Exposure to Local but Not Inhalation Anesthetics Affects Anesthesiology 2005; 102:353–63 © 2005 American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins, Inc. Long-term Exposure to Local but Not Inhalation Anesthetics Affects Neurite Regeneration and Synapse Formation between Identified Lymnaea Neurons Shin Onizuka, M.D.,* Mayumi Takasaki, M.D., Ph.D.,† Naweed I. Syed, Ph.D.‡ Background: General and local anesthetics are used in vari- MOST surgical procedures require either general or local ous combinations during surgical procedures to repair dam- anesthetic treatments, which last from a few minutes to aged tissues and organs, which in almost all instances involve several hours. Although surgical interventions necessi- nervous system functions. Because synaptic transmission re- tate the use of various anesthetic agents, their choices covers rapidly from various inhalation anesthetics, it is gener- Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/102/2/353/357598/0000542-200502000-00018.pdf by guest on 28 September 2021 ally assumed that their effects on nerve regeneration and syn- should be based on the ones with the least deleterious apse formation that precede injury or surgery may not be as effects on neuronal function, nerve regeneration, and detrimental as that of their local counterparts. However, a di- synaptic repair. This information is important in light of rect comparison of most commonly used inhalation (sevoflu- better choices vis-à-vis various agents that are available to rane, isoflurane) and local anesthetics (lidocaine, bupivacaine), vis-à-vis their effects on synapse transmission, neurite regener- date and are used extensively in clinical practices. To ation, and synapse formation has not yet been performed. render such choices feasible, comparable data for the Methods: In this study, using cell culture, electrophysiologic long-term effects on synaptic transmission, regeneration, and imaging techniques on unequivocally identified presynap- and synapse formation are needed; however, with a few tic and postsynaptic neurons from the mollusc Lymnaea, the notable exceptions1–3 for both general and local anes- authors provided a comparative account of the effects of both general and local anesthetics on synaptic transmission, nerve thetics agents, no such data are currently available. regeneration, and synapse formation between cultured neurons. Notwithstanding the fact that various inhalation (such Results: The data show that clinically used concentrations of as sevoflurane, halothane, and isoflurane), intravenous both inhalation and local anesthetics affect synaptic transmis- (propofol, thiopental, and ketamine), and local anes- sion in a concentration-dependent and reversal manner. The thetic agents (such as lidocaine and bupivacaine) per- authors provided the first direct evidence that long-term over- turb nervous system functions by disrupting either syn- night treatment of cultured neurons with sevoflurane and isoflurane does not affect neurite regeneration, whereas both aptic transmission or nerve conductions, their precise lidocaine and bupivacaine suppress neurite outgrowth com- modes of actions vary considerably from preparation to pletely. The soma–soma synapse model was then used to com- preparation.4 Inhalation anesthetics, for example, affect pare the effects of both types of agents on synapse formation. synaptic transmission by either blocking presynaptic The authors found that local but not inhalation anesthetics transmitter release5 or suppressing postsynaptic recep- drastically reduced the incidence of synapse formation. The 6–9 10–12 local anesthetic–induced prevention of synapse formation most tor function at both excitatory and inhibitory 13,14 likely involved the failure of presynaptic machinery, which synapses, and these responses may invoke a variety otherwise developed normally in the presence of both sevoflu- of ion channels and second messengers.13,15–18 Similarly, rane and isoflurane. intravenous anesthetics such as propofol bring about Conclusion: This study thus provides the first comparative, synaptic depression by enhancing either the function of albeit preclinical, account of the effects of both general and ␥ 8,12,19–21 local anesthetics on synaptic transmission, nerve regeneration, -aminobutyric acid receptors or perhaps by sup- 5 and synapse formation and demonstrates that clinically used pressing presynaptic glutamate release. Despite our cur- lidocaine and bupivacaine have drastic long-term effects on rent understanding of the cellular basis of anesthesia, the neurite regeneration and synapse formation as compared with precise mechanisms by which both general and intrave- sevoflurane and isoflurane. nous agents perturb nervous system function remain largely unknown. This limited understanding of how anes- thetics affect neuronal communications in the nervous sys- tem stems from anatomical challenges that are often met in * Research Associate, Calgary Brain Institute, Faculty of Medicine, University of most mammalian preparations where direct cell–cell inter- Calgary, and Department of Anesthesiology, Miyazaki Medical College, University of Miyazaki. † Professor, Department of Anesthesiology, Miyazaki Medical Col- actions are difficult to study unequivocally. Moreover, as lege, University of Miyazaki. ‡ Professor, Calgary Brain Institute, Faculty of Medicine, University of Calgary. compared with their intravenous and inhalation counter- Received from the † Calgary Brain Institute, Faculty of Medicine, University of parts, even less is known about the mechanisms by which Calgary, Calgary, Alberta, Canada, and the * Department of Anesthesiology, local agents affect synaptic transmission during pain, sur- Miyazaki Medical College, University of Miyazaki, Miyazaki, Japan. Submitted for publication July 20, 2004. Accepted for publication October 15, 2004. Supported gery, and functional recovery. by the Canadian Institutes for Health Research, Ottawa, Ontario, Canada, and In addition to some undesired side effects of all acutely Alberta Heritage Foundation for Medical Research, Edmonton, Alberta, Canada. applied anesthetics,22 long-term treatments of neuronal Address reprint requests to Dr. Syed: Department of Cell Biology and Anatomy, 23 24,25 Faculty of Medicine, University of Calgary, 3330 Hospital Drive Northwest, Calgary, tissue with both inhalation and local agents cause Alberta T2N 4N1, Canada. Address electronic mail to: [email protected]. Indi- widespread learning defects and degeneration. Whether vidual article reprints may be purchased through the Journal Web site, www.anesthesiology.org. such long-term (hours to days) exposure of the neuronal Anesthesiology, V 102, No 2, Feb 2005 353 354 ONIZUKA ET AL. tissue to these anesthetics also affects nerve regenera- at the University of Calgary Animal Resource Centre, tion and synapse formation has not yet been determined. Calgary, Alberta, Canada.) In this study, we took advantage of an ideal model preparation in which synaptic transmission between Cell Culture uniquely identified neurons can be investigated at the Cells were isolated individually and cultured as de- level of single presynaptic and postsynaptic neurons. scribed previously.34 Briefly, snails were anesthetized Individually isolated neurons from the mollusc Lymnaea with 10% Listerine (21.9% ethanol, 0.042% menthol; not only regenerate their neurites in cell culture but also Pfizer Inc., New York, NY) solution in normal Lymnaea recapitulate their specific patterns of synapses, which saline (containing 51.3 mM NaCl, 1.7 mM KCl, 4.1 mM are similar to those seen in vivo. This in vitro approach CaCl2, and 1.5 mM MgCl2) buffered to pH 7.9 with using Lymnaea neurons has been used extensively to Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/102/2/353/357598/0000542-200502000-00018.pdf by guest on 28 September 2021 HEPES. The central ring ganglia were removed under decipher both cellular and synaptic mechanisms by sterile conditions and washed with antibiotic saline which various anesthetics affect neuronal function and (40 ␮g/ml gentamycin; two washes, 10 min each). The synaptic transmission.13,26–34 ganglia were then treated with 0.2% trypsin (Sigma type Here, we sought to determine and compare how clin- III; Sigma Chemical Company, St. Louis, MO) for 22 min ically relevant concentrations of inhalation (sevoflurane followed by 0.2% soybean trypsin inhibitor (Sigma type and isoflurane) and local anesthetics (lidocaine and bu- 1-S; Sigma Chemical Company) for 10 min, both in de- pivacaine) affect synaptic transmission and whether fined medium (DM). DM consisted of serum-free 50% these actions involve presynaptic mechanisms, postsyn- L-15 medium with added inorganic salts (40 mM NaCl, aptic mechanisms, or both. Moreover, we provide the 1.7 mM KCl, 4.1 mM CaCl , 1.5 mM MgCl , and 10 mM first direct and comparative account of how inhalation 2 2 HEPES). The pH was adjusted to 7.9 with 1 N NaOH, and and local anesthetics affect neurite regeneration and 20 ␮M gentamycin was added. The enzymatically treated synapse formation. Specifically, our data show that both ganglia were pinned to the bottom of a dissection dish sevoflurane/isoflurane and lidocaine/bupivacaine block that contained 8 ml high-osmolarity DM (DM with cholinergic synaptic transmission between the paired 37.5 mM glucose). presynaptic and postsynaptic neurons. Long-term (over- The cells were isolated by applying gentle suction to a night) sevoflurane/isoflurane treatment of the cultured fire-polished and Sigmacote (Sigma Chemical Company)–
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