Abstract
Generally, it is assumed that heart-rhythm disorders during hypoxia result from the interplay between the autonomic nervous system (ANS) and the direct effect of hypoxia on cardiorespiratory structures of the central nervous system and on the myocardium. Circadian variability in the ANS may substantially influence the electrical stability of the myocardium, and thus it is associated with the preconditioning protective mechanism. We designed our study using anaesthetized Wistar rats (ketamine/xylazine 100 mg/15 mg/kg, i.m., open chest experiments) to evaluate the effect of preconditioning (PC) induced by 1 to 3 cycles (1 PC–3 PC) of asphyxia (5 min. of artificial hypoventilation, VT = 0.5 ml/100 g of b.w., 20 breaths/min.) and reoxygenation (5 min. of artificial ventilation, VT = 1 ml/100 g of b.w., 50 breaths/min.) on the heart rate (HR) during followed exposure 20 minutes of hypoventilation after adaptation to a light-dark (LD) cycle of 12 hours:12 hours. Hypoxic HR increases were only minimally prevented by 1 to 2 PC pre-treatment, particularly during the dark part of the day. A statistically significant HR increase required 3 PC and was seen only in the light part of the day. We concluded that possible ANS participation in asphyxic preconditioning depends not only on the number of preconditioned cycles but also on the LD cycle, when the ANS participation in preconditioning can be effective only in the light (nonactive) period.
Similar content being viewed by others
References
Cinca J., Moya A., Figueras J., Roma F., Rius J., Circadian variations in the electrical properties of the human heart assessed by sequential bedside electrophysiologic testing, Am. Heart J., 1986, 112, 315–321
Meurling C.J., Waktare J.E.P., Holmqvist F., Hedman A., Camm A.J., Olsson S.B., Malik M., Diurnal variations of the dominant cycle length of chronic atrial fibrillation, Am. J. Physiol., 2001, 280, H401–H406
Simantirakis E.N., Chrysostomakis S.I., Marketou M.E., Kochiadakis G.E., Vardakis K.E., Mavrakis H.E., Vardas P., Atrial and ventricular refractoriness in paced patients — circadian variation and its relationship to autonomous nervous system activity, Eur. Heart J., 2001, 22, 2192–2200
Watanabe M., Nakagawa M., Nobe S., Ohie T., Takahashi N., Hara M., Yonemochi H., Ito M., Saikawa T., Circadian variation of short-lasting asymptomatic paroxysmal supraventricular tachycardia, J. Electrocardiol., 2002, 35, 135–138
Reimer K.A., Hill M.L., Jennings R.B., Prolonged depletion of ATP and the adenosine nucleotide pool due to delayed resynthesis of adenine nucleotides following reversible myocardial ischemic injury in dogs, J. Mol. Cell Cardiol., 1981, 13, 229–239
Barber M.J., Effect of time interval between repeated brief coronary artery occlusions on arrhythmias, electrical activity and myocardial blood flow, J. Am. Coll. Cardiol., 1983, 3, 699–705
Murry C.E., Jennings R.B., Reimer K.A., Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium, Circulation, 1986, 74, 1124–1136
Wolfrum S., Schneider K., Heidbreder M., Nienstedt J., Dominiak P., Dendorfer A., Remote preconditioning protects the heart by activating myocardial PKC epsilon-isoform, Cardiovasc. Res., 2002, 55, 583–589
Pell T.J., Baxter G.F., Yellon D.M., Drew G.M., Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels, Am. J. Physiol. 1998, 275, H1542–H1547
Gho B.C., Schoemaker R.G., van den Doel M.A., Duncker D.J., Verdouw P.D. Myocardial protection by brief ischemia in noncardiac tissue, Circulation, 1996, 94, 2193–2200
Liem D.A., Verdouw P.D., Ploeg H., Kazim S., Duncker D.J., Sites of action of adenosine in interorgan preconditioning of the heart, Am. J. Physiol. Heart Circ. Physiol., 2002, 283, H29–H37
Schoemaker R.G., Van Heijningen C.L., Bradykinin mediates cardiac preconditioning at a distance, Am. J. Physiol. Heart Circ. Physiol., 2000, 278, H1571–H1576
Hu C.P., Peng J., Xiao L., Ye F., Deng H.W., Li Y.J., Effect of age on alpha-calcitonin gene-related peptide-mediated delayed cardioprotection induced by intestinal preconditioning in rats, Regul. Pept., 2002, 107, 137–143
Xiao L., Lu R., Hu C.P., Deng H.W., Li Y.J., Delayed cardioprotection by intestinal preconditioning is mediated by calcitonin gene-related peptide, Eur. J. Pharmacol., 2001, 427, 131–135
Tang Z.L., Dai W., Li Y.J., Deng H.W., Involvement of capsaicin-sensitive sensory nerves in early and delayed cardioprotection induced by a brief ischaemia of the small intestine, Naunyn. Schmiedebergs Arch. Pharmacol., 1999, 359, 243–247
Banerjee A., Locke-Winter C., Rogers K.B., Mitchell M.B., Brew E.C., Cairns C.B., Bensard D.D., Harken A.H., Preconditioning against myocardial dysfunction after ischemia and reperfusion by an alpha 1-adrenergic mechanism, Circ. Res., 1993, 73, 656–670
Cohen M.V., Yang X.M., Liu G.S., Heusch G., Downey J.M., Acetylcholine, bradykinin, opioids, and phenylephrine, but not adenosine, trigger preconditioning by generating free radicals and opening mitochondrial K(ATP) channels, Circ. Res., 2001, 89, 273–278
Miyazaki T., Zipes D.P., Protection against autonomic denervation following acute myocardial infarction by preconditioning ischemia, Circ. Res., 1989, 64, 437–448
Pasceri V., Lanza G.A., Patti G., Pedrotti P., Crea F., Maseri A., Preconditioning by transient myocardial ischemia confers protection against ischemiainduced ventricular arrhythmias in variant angina, Circulation, 1996, 94, 1850–1856
Airaksinen K.E., Ylitalo K.V., Peuhkurinen K.J., Ikaheimo M.J., Huikuri H.V., Heart rate variability during repeated arterial occlusion in coronary angioplasty, Am. J. Cardiol., 1995, 75, 877–881
Huikuri H.V., Makikallio T.H., Heart rate variability in ischemic heart disease, Auton. Neurosci., 2001, 90, 95–101
Woo M.A., Stevenson W.G., Moser D.K., Middlekauff H.R., Complex heart rate variability and serum norepinephrine levels in patients with advanced heart failure, J. Am. Coll. Cardiol., 1994, 23, 565–569
Loukogeorgakis S.P., Panagiotidou A.T., Broadhead M.W., Remote Ischemic Preconditioning Provides Early and Late Protection Against Endothelial Ischemia-Reperfusion Injury in Humans: Role of the Autonomic Nervous System, J. Am. Coll. Cardiol., 2005, 46, 450–456
Wu Z.K., Vikman S., Laurikka J., Pehkonen E., Iivainen T., Huikuri H.V., Tarkka M.R., Nonlinear heart rate variability in CABG patients and the preconditioning effect, Eur. J. Cardio-Thor. Surg. 2005, 28, 109–113
Shizukuda Y., Iwamoto T., Mallet R.T., Downey H.F., Hypoxic preconditioning attenuates tunning caused by repeated coronary artery occlusions in the dog heart, Cardiovasc. Res., 1993, 27, 559–564
Svorc P., Bracokova I., Preconditioning by hypoventilation increases ventricular arrhythmia threshold in Wistar rats, Physiol. Res., 2003, 52, 409–416
Prudian F., Gantenbein M., Pelissier A.L., Attolini L., Bruguerolle B., Daily rhythms of the heart rate, temperature and locomotor activity are modified by anaesthetics in rats: A telemetric study, N. S. Arch. Pharmacol., 1997, 355, 774–778
Pelissier A.L., Gantenbein M., Bruguerolle B., Caffeine-induced modification of heart rate, temperature, and motor activity circadian rhythms in rat, Physiol. Behav., 1998, 67, 81–88
Gantenbein M., Attolini L., Bruguerolle B., Nicorandil affect diurnal rhythms of body temperature, heart rate and locomotor activity in rats, Eur. J. Pharmacol., 1998, 346, 125–130
Svorc P., Bracokova I., Bacova I., Svorcova E., Acidbase balance and artificial controlled ventilation in Wistar rats: Chronobiological view. Abstract Book from The Third International Congress of Applied Chronobiology and Chronomedicine, 2009, Akko, Israel, p. 67 (abstract)
Jarsky T.M., Stephenson R., Effects of hypoxia and hypercapnia on circadian rhythms in the golden hamster (Mesocricetus auratus), J. Appl. Physiol., 2000, 89, 2130–2138
Mortola J.P., Seifert E.L., Hypoxic depression of circadian rhythms in adult rats, J. Appl. Physiol., 2000, 88, 365–368
Bishop B., Silva G., Krasney J., Nakano H., Roberts A., Farkas G., Rifkin D., Shucard D., Ambient temperature modulates hypoxic-induced changes in rat body temperature and activity differentially, Am. J. Physiol., 2001, 280, R1190–R1196
Bosco G., Ionadi A., Panico S., Faralli F., Gagliardi R., Data P., Mortola J.P., Effects of hypoxia on the circadian patterns in men, High Alt. Med. Biol., 2003, 4, 305–318
Kaplan J.L., Gao E., DeGaravilla L., Victain M., Minczak B., Dalsey W.C., Adenosine A1 antagonism attenuates atropine-resistant hypoxic bradycardia in rats, Acad. Emerg. Med., 2003, 10, 923–930
Chanine R., Adam A., Yamaguchi N., Gaspo R., Regoli D., Nadeau R., Protective effects of bradykinin on the ischaemic heart: implication of the B1 receptor, Br. J. Pharmacol., 1993, 108, 318–322
Ohkuwa T., Itoh H., Yamamoto T., Minami C., Yamazaki Y., Effect of hypoxia on norepinephrine of various tissues in rats, Wilderness. Environ. Med., 2005, 16, 22–26
Kawaguchi T., Tsubone H., Hori M., Ozaki H., Kuwahara M., Cardiovascular and autonomic nervous function during acclimatization to hypoxia in conscious rats, Auton. Neurosci., 2005, 117, 94–104
Hayashida Y., Hirakawa H., Nakamura T., Maeda M., Chemoreceptors in autonomic responses to hypoxia in conscious rats. In: Zapata et al. (Eds.) Frontiers in Arterial Chemoreception, Plenum Press, New York, pp. 439–442, 1996
Hinojosa-Laborde C., Mifflin S.W., Sex differences in blood pressure response to intermittent hypoxia in rats, Hypertension, 2005, 46, 1016–1021
Kamasaki Y., Guo A.C., McDonald T.F., Protection by hypoxic preconditioning against hypoxiareoxygenation injury in guinea-pig papillary muscles, Cardiovasc. Res., 1997, 34, 313–322
Ravingerova T., Løkebø J.E., Munch-Ellingsen J., Sundset R., Tande P., Ytrehus K., Mechanism of hypoxic preconditioning in guinea pig papillary muscles, Mol. Cell Biochem., 1998, 186, 53–60
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Svorc, P., Bacova, I., Benacka, R. et al. Heart-rate changes in asphyxic preconditioning in rats depend on light-dark cycle. cent.eur.j.med 6, 312–319 (2011). https://doi.org/10.2478/s11536-011-0021-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11536-011-0021-5