The effect of hyperbaric oxygenation on cardiodynamics and oxidative stress in rats with sepsis

Aleksandar Jevtić; Vladimir Živković; Milica Milinković; Željko Mijailović; Nevena Draginić; Marijana Andjić; Andjela Milojević Šamanović; Sergey Bolevich; Vladimir Jakovljević

doi:10.2298/VSP191026142J

Aleksandar Jevtić Institute for Orthopedic Surgery “Banjica”, Belgrade, Serbia
Vladimir Živković University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia
Milica Milinković University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia
Željko Mijailović University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Nevena Draginić University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Marijana Andjić University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Andjela Milojević Šamanović Department of Dentistry, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia
Sergey Bolevich 1st Moscow State Medical University IM Sechenov, Department of Human Pathology, Moscow, Russian Federation
Vladimir Jakovljević University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia

DOI: https://doi.org/10.2298/VSP191026142J

Keywords: hyperbaric oxygenation, oxidative stress, sepsis, heart, rats

Abstract

Background/Aim. Dysfunctions at the cellular, tissue, and organ level, which can result in death, are caused by metabolic changes and affection on the regulation of gene transcription and micro- and macrocirculation. The aim of the present study was to assess the impact of hyperbaric oxygenation (HBO) on isolated heart as well as on the oxidative status of rats with sepsis. Methods. The investigation included male Wistar albino rats classified into three groups: the first group was a control group (CTRL); the second group included animals exposed only to the induction of sepsis without HBO treatment (the Sepsis group), while the third group included animals treated with HBO after the induction of sepsis (the Sepsis + HBO group). For the induction of sepsis, fecal peritonitis model was used (3 mL/kg of fecal suspension administered intraperitoneally). After the induction of sepsis, the rats were exposed twice a day (on 12 hours) to HBO treatment at 2.8 atmospheres absolute (ATA) for 90 minutes over a period of 3 days. 72 h after the confirmation of sepsis, the animals were sacrificed and the hearts were retrogradely perfused on the Langendorff apparatus at a gradually increased coronary perfusion pressure (CPP = 40–120 cm H₂O). The following parameters of heart function were continuously recorded: maximum and minimum rate of left ventricular pressure development (dp/dt max, dp/dt min); systolic and diastolic left ventricular pressure (SLVP and DLVP); heart rate (HR). Coronary flow (CF) was measured flowmetrically. Following oxidative stress markers were measured: nitrites (NO₂⁻), superoxide anion radical (O₂⁻), hydrogen peroxide (H₂O₂), index of lipid peroxidation (TBARS), activity of superoxide dismutase (SOD) and catalase (CAT) and the level of reduced glutathione (GSH). Results. There were no significant differences in dp/dt max, dp/dt min, SLVP and HR between the groups. CF was statistically significantly higher (p < 0.01) in the sepsis group. The values of all cardiac oxidative markers were lower in the sepsis + HBO group (p < 0.05), while systemic pro-oxidative and antioxidative parameters were unchanged. Conclusion. Our results showed that HBO treatment was not associated with improved cardiac function and coronary perfusion, while expressed promising beneficial effects on cardiac oxidative stress.

Author Biography

Vladimir Živković, University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia

References

Gyawali B, Ramakrishna K, Dhamoon AS. Sepsis: The evolution in definition, pathophysiology, and management. SAGE Open Med 2019; 7: 2050312119835043.

Manfredini A, Constantino L, Pinto MC, Michels M, Burger H, Kist LW, еt al. Mitochondrial dysfunction is associated with long-term cognitive impairment in an animal sepsis model. Clin Sci (Lond) 2019; 133(18): 1993–2004.

Rello J, Valenzuela-Sánchez F, Ruiz-Rodriguez M, Moyano S. Sep-sis: A review of advances in management. Adv Ther 2017; 34(11): 2393–411.

Fattahi F, Ward PA. Complement and sepsis-induced heart dysfunction. Mol Immunol 2017; 84: 57–64.

Gupta A, Brahmbhatt S, Kapoor R, Loken L, Sharma AC. Chron-ic peritoneal sepsis: myocardial dysfunction, endothelin and signaling mechanisms. Front Biosci 2005; 10: 3183–205.

Chopra M, Sharma AC. Distinct cardiodynamic and molecular characteristics during early and late stages of sepsis-induced myocardial dysfunction. Life Sci 2007; 81(4): 306–16.

Chopra M, Sharma AC. Apoptotic cardiomyocyte hypertrophy during sepsis and septic shock results from prolonged exposure to endothelin precursor. Front Biosci 2007; 12: 3052–60.

Babul S, Rhodes EC. The role of hyperbaric oxygen therapy in sports medicine. Sports Med 2000; 30(6): 395–403.

Poff AM, Kernagis D, D'Agostino DP. Hyperbaric environment: oxygen and cellular damage versus protection. Compr Physiol 2016; 7(1): 213–34.

Bennett M, Best TM, Babul S, Taunton J, Lepawsky M. Hyperbar-ic oxygen therapy for delayed onset muscle soreness and closed soft tissue injury. Cochrane Database Syst Rev 2005; (4): CD004713.

Demchenko IT, Zhilyaev SY, Moskvin AN, Krivchenko AI, Pian-tadosi CA, Allen BW. Baroreflex-mediated cardiovascular re-sponses to hyperbaric oxygen. J Appl Physiol 2013; 115(6): 819–28.

Bergo GW, Tyssebotn I. Cardiovascular effects of hyperbaric oxygen with and without addition of carbon dioxide. Eur J Appl Physiol Occup Physiol 1999; 80(4): 264–75.

Halbach JL, Prieto JM, Wang AW. Early hyperbaric oxygen therapy improves survival in a model of severe sepsis. Am J Physiol Regul Integr Comp Physiol 2019; 317(1): R160–8.

Tai PA, Chang CK, Niu KC, Lin MT, Chiu WT, Lin JW. Re-duction of ischemic and oxidative damage to the hypothala-mus by hyperbaric oxygen in heatstroke mice. J Biomed Bio-technol 2010; 2010: 609526.

Zolfaghari PS, Pinto BB, Dyson A, Singer M. The metabolic phe-notype of rodent sepsis: cause for concern? Intensive Care Med Exp 2013; 1(1): 25.

Ozturk А, Yamanel L, Ozenc S, Ince M, Simsek K, Comert B, et al. Comparison of the effects of hyperbaric oxygen and nor-mobaric oxygen on sepsis in rats. Arch Clin Exp Surg 2016; 5(1): 7–12.

Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 1982; 126(1): 131–8.

Pick E, Keisari Y. A simple colorimetric method for the meas-urement of hydrogen peroxide produced by cells in culture. J Immunol Methods 1980; 38(1‒2): 161–70.

Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in ani-mal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95(2): 351–8.

Auclair C, Voisin E. Nitroblue tetrazolium reduction. In: Greenvvald RA, editor. Handbook of methods for oxygen radi-cal research. Boca Raton: CRC Press; 1985. p. 123–32.

McCord JM, Fridovich I. The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the in-teraction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem 1969; 244(22): 6056–63.

Misra HP, Fridovich I. The role of superoxide-anion in the au-tooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972; 247(10): 3170–5.

Beutler E. Catalase. In: Beutler E editor. Red cell metabolism, a manual of biochemical methods. New York, NY, USA: Grune and Stratton; 1982. p. 105–6.

Beutler E. Reduced glutathione (GSH). In: Beutler E editor. Red cell metabolism, a manual of biochemical methods. New York, NY, USA: Grune and Stratton; 1975. p. 112–4.

Zhai X, Yang Z, Zheng G, Yu T, Wang P, Liu X, et al. Lactate as a potential biomarker of sepsis in a rat cecal ligation and puncture model. Mediators Inflamm 2018; 2018: 8352727.

Drosatos K, Lymperopoulos A, Kennel PJ, Pollak N, Schulze PC, Goldberg IJ. Pathophysiology of sepsis-related cardiac dysfunc-tion: driven by inflammation, energy mismanagement, or both? Curr Heart Fail Rep 2015; 12(2): 130–40.

de Montmollin E, Aboab J, Mansart A, Annane D. Bench-to-bedside review: beta-adrenergic modulation in sepsis. Crit Care 2009; 13(5): 230.

Drosatos K, Khan RS, Trent CM, Jiang H, Son NH, Blaner WS, et al. Peroxisome proliferator-activated receptor-γ activation prevents sepsis-related cardiac dysfunction and mortality in mice. Circ Heart Fail 2013; 6(3): 550–62.

Yang ZJ, Bosco G, Montante A, Ou XI, Camporesi EM. Hyper-baric O2 reduces intestinal ischemia-reperfusion-induced TNF-alpha production and lung neutrophil sequestration. Eur J Appl Physiol 2001; 85(1‒2): 96–103.

Chang KY, Tsai PS, Huang TY, Wang TY, Yang S, Huang CJ. HO-1 mediates the effects of HBO pretreatment against sep-sis. J Surg Res 2006; 136(1): 143–53.

Rudiger A, Dyson A, Felsmann K, Carré JE, Taylor V, Hughes S, et al. Early functional and transcriptomic changes in the myo-cardium predict outcome in a long-term rat model of sepsis. Clin Sci (Lond) 2013; 124(6): 391–401.

Lin HC, Wan FJ, Wu CC, Tung CS, Wu TH. Hyperbaric oxy-gen protects against lipopolysaccharide-stimulated oxidative stress and mortality in rats. Eur J Pharmacol 2005; 508(1‒3): 249–54.

Edremitlioğlu M, Kiliç D, Oter S, Kisa U, Korkmaz A, Coşkun O, et al. The effect of hyperbaric oxygen treatment on the renal functions in septic rats: relation to oxidative damage. Surg Today 2005; 35(8): 653–61.

Oter S, Edremitlioglu M, Korkmaz A, Coskun O, Kilic D, Kisa U, et al. Effects of hyperbaric oxygen treatment on liver func-tions, oxidative status and histology in septic rats. Intensive Care Med 2005; 31(9): 1262–8.

Bektas A, Ulusoy M, Mas MR. Do late phase hyperbaric and normobaric oxygen therapies have effect on liver damage? An experimental sepsis model. Gen Med (Los Angel) 2019; 7(1): 324.