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Resuscitation of Hypoxic Newborn Piglets with Oxygen Induces a Dose-Dependent Increase in Markers of Oxidation

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Resuscitation of Hypoxic Newborn Piglets with Oxygen Induces a Dose-Dependent Increase in Markers of Oxidation 0031-3998/00/6205-0559 PEDIATRIC RESEARCH Vol. 62, No. 5, 2007 Copyright © 2007 International Pediatric Research Foundation, Inc. Printed in U.S.A. Resuscitation of Hypoxic Newborn Piglets With Oxygen Induces a Dose-Dependent Increase in Markers of Oxidation RØNNAUG SOLBERG, JANNICKE H. ANDRESEN, RAQUEL ESCRIG, MAXIMO VENTO, AND OLA DIDRIK SAUGSTAD Department of Pediatric Research [R.S., J.H.A., O.D.S.], Medical Faculty, University of Oslo Rikshospitalet Medical Centre, Oslo, N-0027, Norway; Servicio de Neonatologı´a [R.E., M.V.], Hospital Universitario Materno-Infantil La Fe, Valencia, 46009, Spain ABSTRACT: Newborn resuscitation with pure oxygen may be of childhood leukemia and cancer (5,6) making it mandatory associated with long-term detrimental effects. Due to the change in to search for the causal connection. attitude toward use of less oxygen upon resuscitation, there is a need We wanted to explore possible reasons for long-term effects to study effects of intermediate hyperoxia. The aim was to study of oxidative stress as well as to search for signs of oxidative dose-response correlation between inspiratory fraction of oxygen damage to DNA and proteins and have chosen two biomarkers used for resuscitation and urinary markers of oxidative damage to of oxidative stress; 8-hydroxy-2=-deoxyguanosine (8oxodG) DNA and amino acids. Hypoxemia was induced in newborn piglets and ortho-tyrosine (o-Tyr). Urinary excretion of modified following a standardized model; they were resuscitated for 15 min nucleosides/bases i.e., 8oxodG can be measured to assess with either 21%, 40%, 60% or 100% oxygen and observed for 1 h. Urine samples were collected. Urinary elimination of 8-hydroxy-2=- oxidative damage on the level of the whole organism (7) and deoxyguanosine (8-oxo-dG), 2=deoxyguanosine (2dG), ortho- has been used to evaluate oxidative stress in patients (8). O-tyr tyrosine (o-Tyr) and phenylalanine (Phe) were determined by HPLC is known to be formed entirely upon reaction of Phe with and tandem mass spectrometry (HPLC-MS/MS). Quotient of 8-oxo-dG/ hydroxyl radicals and can also be measured in urine (9). 2dG and o-Tyr/Phe ratios were significantly and dose-dependant higher In addition, we also wanted to study the effect of re oxy- in piglets resuscitated with supplementary oxygen. 8-oxodG/dG: Mean genation with different oxygen concentrations to see if there is (SD) 5.76 (1.81) versus 22.44 (12.55) p Ͻ 0.01 and o-Tyr/Phe: 19.07 a dose-dependency or if there could be a threshold beyond (10.7) versus 148.7 (59.8)for 21% versus 100%, p Ͻ 0.001. Hypoxia which supplementary oxygen seems to be detrimental. and subsequent resuscitation for 15 min with graded inspiratory We hypothesized that resuscitation of piglets with supple- fraction of oxygen causes increased oxidative stress and a dose- mentary oxygen (40%, 60% or 100%) would cause increased dependant oxidation of DNA and Phenylalanine. The increase in the oxidative stress, more reactive oxygen species (ROS), and hydroxyl attack may lead to a pro-oxidative status and risk for more damage to proteins and DNA than 21% oxygen. genetic instability. (Pediatr Res 62: 559–563, 2007) he transition from fetal to neonatal life contains complex MATERIALS AND METHODS Tand rapid physiologic changes. Usually, these changes are spontaneous, but approximately 10% of newborn babies re- The National Animal Research Authority, (NARA), approved the experi- quire some assistance to begin breathing, and about 1% mental protocol. The animals were cared for and handled in accordance with the European Guidelines for Use of Experimental Animals. requires extensive resuscitation (1). Surgical preparation and anesthesia. Thirty-eight newborn Noroc Compared with the intrauterine pO2 at about 3.3 kPa every (LYxLD) pigs (20 male, 18 female) were included in this study, inclusion child comes out to a relative hyperoxia and the values will criteria being 12–36 h, Hb Ͼ5g/dL and good general condition. The piglets were anaesthetized, tracheotomized, ventilated and surgically prepared as normally spontaneously rise to about 8kPa during the first 30 previously described by Munkeby et al. (10). min pp. Excessive hyperoxia may disturb a tuned equilibrium Experimental Protocol. The animals were stabilized for one hour after the in the oxidative-antioxidative system. Exposure to hyperoxia initial procedures. Hypoxemia was induced by ventilation of 8% O2 in N2 and maintained until Base Excess (BE) reached -20 mmol/L or mean arterial generates significant higher levels of free radicals, and even blood pressure (MABP) decreased to 15 mm Hg. The saline infusion was more when preceded by hypoxia (2). stopped and CO2 was added during the whole duration of the hypoxemia aiming at a PaCO level of 8.0–9.5 kPa. Before start of resuscitation, piglets In the neonatal literature an increasing number of studies 2 were randomized into four different groups. Thus, they were resuscitated for focusing on supplementary oxygen shows how oxidative 15 min by ventilation with either 21% (n ϭ 8), 40% (n ϭ 9), 60% (n ϭ 8) or stress influences both mortality and morbidity (3,4). More- 100% (n ϭ 6) oxygen. Thereafter, they were observed for 60 min, ventilated over, babies exposed to high oxygen concentrations in the first with 21% oxygen, before receiving a lethal dose of pentobarbital (150 mg/kg iv). The abdominal wall was opened and the urine collected through direct minutes of postnatal life have been shown to be at higher risk aspiration from the visible bladder, and immediately snap frozen on liquid Received May 7, 2007; accepted June 19, 2007. Abbreviations: 8-oxodG, 8-hydroxy-2=-deoxyguanosine; dG, 2=deoxyguanosine; Correspondence: Rønnaug Solberg, MD, Department of Pediatric Research Medical HPLC-MS/MS, high-performance liquid chromatography and tandem mass Faculty, University of Oslo, Rikshospitalet-Radiumhospitalet Medical Center, 0027 Oslo, Norway; e-mail: [email protected] spectrometry; o-Tyr, ortho-tyrosine; Phe, phenylalanine; ROS, reactive ox- This work was supported by Helse Sor. ygen species 559 560 SOLBERG ET AL. nitrogen and stored at minus 70°C. Laboratory personnel were blinded to the these protonated molecules. Calibration curves were obtained using a standard percentage oxygen administered, the study staff not. (0.001–10 ␮M) and were in each case found to be linear with correlation Seven piglets, referred to as baseline pigs, were SHAM operated controls coefficients Ͼ0.99. The limits of detection and quantitation for our method that went through surgery and1hofstabilization on ventilator and they were were of 0.001 ␮M. not exposed to hypoxia and reoxygenation (by drawing lots). Statistics. SPSS 13 for Windows® was used for the baseline characteristics High performance liquid chromatography and mass spectrometry. De- of the piglets. Statistical analysis was performed in two steps. One-way termination of ortho-tyrosine (o-Tyr), phenylalanine (Phe), 8-hydroxy-2=- analysis of variance (ANOVA) was performed first. When the overall com- deoxyguanosine (8-oxodG) and 2=-deoxyguanosine (dG) in urine by High parison of groups was significant, differences between individual groups were Performance Liquid Chromatography and Mass Spectrometry (HPLC-MS/MS). investigated by Tukey’s method. Differences were considered to be significant HPLC-MS/MS was carried out using a Quattro Micro triple-quadruple at p Ͻ 0.05. Nonparametric statistics (Mann Whitney’s U test) for comparison mass spectrometer (Micromass, Manchester, UK) equipped with a Shimadzu of nonpaired samples were used for the HPLC-MS/MS results, as data did not LC-10ADvp. pump and a SLC-10Avp. Controller system with a SIL- show normal distribution. 10ADvp. auto injector. Samples were analyzed by reverse-phase HPLC using a Phenomenex (Torrance, CA) Prodigy ODS column (100 ϫ 2 mm) with 3-␮m particle size. In all cases 30 ␮L were injected onto the column. The RESULTS temperature of the column was maintained at 25°C. The following gradient Ϯ system, pumped through the column at 0.2 mL/min, was used (min/%A/%B) The piglets had a mean (SD), weight of 1798 ( 198) (A, 0.1% formic acid; B, methanol): 0/95/5, 10/95/5, 15/95/5, 15.1/95/5, grams, Hb was 7.5 (Ϯ1.1) g/dL and the mean time of hypox- 30/95/5. Positive ion electro spray tandem mass spectra were recorded with emia was 60.3 (Ϯ34.3) min. These variables were not statis- the electro spray capillary set at 3.5 keV and a source block temperature of 120°C. Nitrogen was used as the drying and nebulising gas at flow rates of tically different between the groups. The arterial blood gases 300 and 30 L/h, respectively. Argon at 1.5 ϫ 10Ϫ3 mbar was used as the are provided in Table 1. collision gas for collision-induced dissociation. An assay based on HPLC- Both 8-oxodG and o-tyrosine showed a dose-dependant MS/MS with multiple reaction monitoring was developed using the transi- tions m/z 182¡136 for o-Tyr, 166¡120 for Phe, 284¡168 for 8-oxodG, and increase according to the oxygen concentration used upon 268¡152 for dG, all of which represent favorable fragmentation pathways for resuscitation (Table 2). The values should be expressed as a Table 1. Arterial blood gas values End 15 min 20 min after 60 min after Group Baseline End hypoxia resuscitation resuscitation resuscitation pH 21% 7.5 (0.4) 7.0 (0.1) 7.1 (0.2) 7.3 (0.1) 7.4 (0.8) 40% 7.5 (0.8) 6.9 (0.6) 7.1 (1.0) 7.2 (0.1) 7.3 (0.6) 60% 7.4 (0.1) 6.9 (0.1) 7.1 (0.2) 7.2 (0.1) 7.4 (0.2) 100% 7.5 (0.3) 6.9 (0.1) 7,0 (0.1) 7.1 (0.1) 7.3 (0.1) Control 7.5 (0.1) 7.5 (0.1) pO2 (kPa) 21% (1.9)
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