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Nitrous Oxide Revisited Anesthesiology 2005; 103:845–54 © 2005 American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins, Inc. Nitrous Oxide Revisited Evidence for Potent Antihyperalgesic Properties Philippe Richebe´ , M.D., Ph.D.,* Cyril Rivat, Ph.D.,† Cyril Creton, M.Sc.,† Jean-Paul Laulin, Ph.D.,‡ Pierre Maurette, M.D., Ph.D.,§ Marc Lemaire, M.D.,࿣ Guy Simonnet, Ph.D.# Background: Although opioids are unsurpassed analgesics NITROUS oxide is commonly used in humans for pain for surgery, they also induce an N-methyl-D-aspartate–depen- relief. Experimental animal studies have revealed that dent enhancement of postoperative hyperalgesia. Because ni- nitrous oxide induces opioid peptide release in the peri- trous oxide (N2O) has anti–N-methyl-D-aspartate properties, the purpose of this study was to evaluate nitrous oxide ability to aqueductal brainstem, leading to disinhibition (activa- prevent such an opioid-induced hyperalgesia in rats. tion) of the descending noradrenergic inhibitory path- Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/103/4/845/360312/0000542-200510000-00024.pdf by guest on 01 October 2021 ␥ Methods: First, preventive effects of 50/50% N2O–O2 on the ways via inhibition of -aminobutyric acid–mediated development of delayed hyperalgesia observed after inflamma- interneurons. This results in a negative modulation of the 1–3 tory pain (hind paw carrageenan injection on D0) were exam- nociceptive processes at the spinal cord level. ined for several days. Second, the ability of nitrous oxide (10– A challenging hypothesis is that the nitrous oxide an- 40%) to limit opioid-induced hyperalgesia induced by fentanyl algesic effect is not limited to its antinociceptive effect was evaluated in nonsuffering rats. Third, antihyperalgesic ef- fects of various nitrous oxide concentrations (20–50%) were via endogenous opioids systems but may also be due to assessed in both inflammatory and incisional pain models in the preventive blockade of pain hypersensitivity induced fentanyl-treated rats (4 ؋ 100 ␮g/kg subcutaneously). Finally, by nociceptive inputs. It is generally recognized that the analgesic effect of a single dose of morphine was evaluated tissue damage associated with surgical lesions or inflam- 24 h after fentanyl administration and nitrous oxide (D )to 0 mations often produces peripheral and central sensitiza- assess its preventive effect on acute morphine tolerance in both tion that may outlast the stimuli leading to sustained nonsuffering and hind paw–incised rats. hyperalgesia, allodynia, and persistent pain.4–7 At the Results: When applied on D0, nitrous oxide reduced delayed hyperalgesia induced by inflammation. Exposure to nitrous central level, many experimental studies have shown a oxide on D0 also reduced opioid-induced hyperalgesia in non- critical role for excitatory amino acids to injury-induced suffering rats in a dose-dependent manner. In fentanyl-treated pain sensitization via N-methyl-D-aspartate (NMDA) re- rats with inflammatory or incisional pain, nitrous oxide strongly ceptors. Because the aim of preemptive analgesia is to limited both magnitude and duration of hyperalgesia. Moreover, reduce central sensitization that arises from surgical nox- nitrous oxide exposure on D opposed development of acute tol- 0 ious inputs, many clinical studies have evaluated the erance to analgesic effects of morphine administered on D1 in both nonsuffering and incised fentanyl-treated rats. effectiveness of several NMDA receptor antagonists for Conclusions: Nitrous oxide, an N-methyl-D-aspartate receptor improving postoperative pain management. Clinical antagonist, prevented the enhancement of pain sensitivity in- studies using intravenous low doses of NMDA receptor duced by both nociceptive inputs and fentanyl and opposed antagonists have reported controversial results in hu- acute morphine tolerance. Results suggest that perioperative mans.8 However, ketamine and dextromethorphan have nitrous oxide use reduces exaggerated postoperative pain and morphine consumption. demonstrated promising antihyperalgesic effects in sev- eral clinical trials leading to a reduction in both postop- erative pain and morphine consumption.9–11 Because nitrous oxide was recently shown to be an * Staff Anesthesiologist, Department of Anesthesia and Intensive Care II, 12 Centre Hospitalier et Universitaire de Bordeaux, Bordeaux, France. Ph.D. Stu- NMDA receptor antagonist, one hypothesis is that ni- dent, Laboratoire Home´ostasie-Allostasie-Pathologie EA3666, Universite´ Victor trous oxide should have beneficial antihyperalgesic Se´galen-Bordeaux 2. † Staff Researcher, # Professor, Laboratoire Home´ostasie- Allostasie-Pathologie EA3666, Universite´ Victor Se´galen-Bordeaux 2. ‡ Assistant properties mimicking the ketamine ones, especially Professor Universite´ Bordeaux 1, Bordeaux, France. § Professor, Department of when large opioid doses are used during surgery. Exper- Anesthesia and Intensive Care III, Centre Hospitalier et Universitaire de Bor- 13–18 19–21 deaux, Bordeaux, France. ࿣ M.D., Medical Gases Domain Director, Research and imental and clinical studies have reported that Development, Claude-Delorme Research Center, Air Liquide, Jouy-en-Josas, opioids may paradoxically facilitate the activation of France. NMDA-dependent pronociceptive systems leading to ex- Received from the Laboratoire Home´ostasie-Allostasie-Pathologie EA3666, Uni- versite´ Victor Segalen-Bordeaux 2, Bordeaux, France. Submitted for publication aggerated postoperative pain. March 22, 2005. Accepted for publication July 2, 2005. Supported by the The purpose of the current study was to evaluate the Universite´ Victor Segalen Bordeaux 2, Bordeaux, France; the Ministe`re de l’Education nationale, de l’Enseignement supe´rieur et de la Recherche, Paris, nitrous oxide potency for preventing pain sensitization France; the Conseil Re´gional d’Aquitaine, Bordeaux, France; and Air Liquide induced by nociceptive inputs and high doses of fenta- Research and Development, Jouy-en-Josas, France. Presented at the Annual Meet- 16–18 ings of the Socie´te´ Franc¸aise d’Anesthe´sie et Re´animation, Paris, France, Septem- nyl. To assess such a hypothesis, we first evaluated ber 19, 2003, and the American Society of Anesthesiologists, San Francisco, the effect of a 50/50% N O–O mixture in rats with October 13, 2003. 2 2 inflammatory pain induced by a unilateral hind paw Address reprint requests to Dr. Simonnet: Laboratoire Home´ostasie-Allostasie- Pathologie EA3666, Universite´ Victor Segalen-Bordeaux 2, 146, rue Le´o Saignat, injection of the proinflammatory drug carrageenan. Sec- 33076 Bordeaux Cedex, France. Address electronic mail to: [email protected]. Individual article reprints may be purchased through the Journal Web site, www. ond, we tested the effects of different nitrous oxide anesthesiology.org. concentrations on the development of hyperalgesia in- Anesthesiology, V 103, No 4, Oct 2005 845 846 RICHEBE´ ET AL. duced by high doses of fentanyl in nonsuffering rats. sliding door on one side to insert rats. Five rats were Third, we evaluated preventive effects of different ni- introduced in each chamber. Fresh gases were fed into trous oxide concentrations on the fentanyl enhancement the chamber through an inlet port (4 l/min) and purged of hyperalgesia induced by inflammatory or incisional by a vacuum set for sucking out the gas at the same rate nociceptive stimuli. Fourth, the 50/50% N2O–O2 mix- as the fresh gas inflow. Oxygen and nitrous oxide con- ture perioperative use was tested for evaluating its effec- centrations were continuously monitored to confirm the tiveness to prevent acute morphine tolerance observed gases’ concentrations. All gas exposures were initiated after such a hind paw surgery associated with perioper- 15 min before the beginning of each experiment and ative high doses of fentanyl.18 were followed for4hofexposure. The total gas expo- sure time was4h15min. Materials and Methods Measurement of Nociceptive Threshold Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/103/4/845/360312/0000542-200510000-00024.pdf by guest on 01 October 2021 Animals Nociceptive thresholds in handheld rats were deter- Experiments were performed on adult male Sprague- mined by a modification of the Randall-Selitto method,22 Dawley rats (Charles River Laboratories, l’Abresle, the paw-pressure vocalization test, in which a constantly France) weighing 300–350 g, housed in groups of five increasing pressure is applied to the hind paw until the per cage with a 12-h light–12-h dark cycle (lights on at rat squeaks. The Basile analgesimeter (Apelex, Massy, 7:00 AM) at a constant room temperature of 23° Ϯ 2°C. France; stylus tip diameter, 1 mm) was used. A 600-g The animals had access to food and water ad libitum. cutoff value was determined to prevent tissue damage. Pharmacologic tests and care of the animals were con- ducted in accordance with the Animals Care and Use Carrageenan Injection manual of the National Institutes of Health (Bethesda, On D0, the basal value of the nociceptive threshold MD, National Institutes of Health, 1999). This study, was evaluated, and rats were placed in a plastic cage and including care of the animals involved, was conducted then anesthetized with 3% halothane for 3 min. Carra- according to the official edict presented by the French geenan (0.2 ml of a 1% carrageenan solution in saline) was Ministry of Agriculture (Paris, France) and the recom- then injected into one rat plantar hind paw subcutane- mendations of the Helsinki Declaration.
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