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Lipid Peroxidation in Newborn Rabbits: Effects of Oxygen, Lipid Emulsion, and Vitamin El

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Lipid Peroxidation in Newborn Rabbits: Effects of Oxygen, Lipid Emulsion, and Vitamin El 003 1-3998/86/2006-0505$02.00/0 PEDIATRIC RESEARCH Vol. 20, No. 6, 1986 Copyright O 1986 International Pediatric Research Foundation, Inc. Printed in U.S.A. Lipid Peroxidation in Newborn Rabbits: Effects of Oxygen, Lipid Emulsion, and Vitamin El JON R. WISPE,~MATTHEW KNIGHT,' AND ROBERT J. ROBERTS Division of Neonatology, Department of Pediatrics, University of lowa, College of Medicine, Iowa City, Iowa 52242 ABSTRACT. The extent of in vivo lipid peroxidation and with hyperoxic exposure, including bronchopulmonary dysplasia the in vivo antioxidant effects of a-tocopherol and a- and retrolental fibroplasia. tocopheryl acetate were studied in newborn rabbits exposed The exact mechanism by which oxidant tissue damage occurs to one of two oxidant stresses: hyperoxia (FIO~>0.9) or is not clear. Several lines of evidence support the hypothesis that parenteral lipid emulsion infusion. Lipid peroxidation was oxidant injury is mediated by the generation of partially reduced monitored by measurement of expired ethane and pentane, oxygen species (1-3). These reactive species may damage tissues tissue thiobarbituric acid (TBA) reactants, and tissue lipid by peroxidation of lipids, oxidation of proteins and nucleic acids, peroxides. Seventy-two h of hyperoxia did not increase any or through yet undefined mechanisms. It has long been presumed of the parameters of lipid peroxidation although mortality that polyunsaturated fatty acids in membranes are particularly was higher in oxygen exposed animals. a-Tocopherol (100 susceptible to oxidative processes, and that "lipid peroxidation" mg/kg, intravenous) lowered expired hydrocarbons and is a central feature of oxygen-associated tissue damage. Lipid tissue TBA reactants, but raised liver lipid peroxides in peroxidation is associated with the generation of lipid-derived both air and hyperoxia exposed pups. Infusion of soybean intermediate products including lipid hydroperoxides, hydroxy- oil emulsion increased production of ethane and pentane, aldehydes, and malonaldehyde. These intermediates may be liver TBA reactants, and lung lipid peroxides. Both a- important in the damage process, because they also are very tocopherol and a-tocopheryl acetate prevented the soybean reactive and can propagate further oxidizing reactions (4). oil emulsion induced increase in volatile hydrocarbons. a- The mature human organism vossesses vrotective mechanisms Tocopherol (100 mg/kg, intravenous) administration also to detoxify both reactive Exygen metabolites and the lipid-derived prevented the increase in liver TBA reactants and lung intermediates. These include enzymatic (superoxide dismutase, lipid peroxides. In identically treated animals, a-tocopheryl catalase, and the glutathione system) and nonenzymatic factors acetate administration decreased liver TBA reactants but (sulfhydryl containing amino acids and vitamins E and C) (3). had no effect on lung lipid peroxides. We conclude that a- In the newborn, particularly the preterm newborn, protective tocopherol reduces lipid peroxidation in newborn rabbits systems may not be fully active, in part because the nutritional including animals exposed to hyperoxia or infused with sources of antioxidant vitamins and necessary cofactors for the lipid emulsions. a-Tocopheryl acetate results in lower tis- protective enzymes are insufficient (5, 6). Despite these "defi- sue a-tocopherol concentrations and is less effective as an ciencies," most newborn animal species appear to be resistent to antioxidant in lipid emulsion infused rabbits. (Pediatr Res oxygen-induced toxicities (7). However, the conclusion that new- 20: 505-510,1986) borns are resistant to oxidative injury is based on mortality data which may not reflect the importance of vitamin E and the Abbreviations antioxidant enzyme systems to individual tissues or organs. For example, newborn animals suffer severe lung damage after ex- TBA, thiobarbituric acid posure to hyperoxia (9, and their resistence to oxygen-related LOOH, lipid hydroperoxides mortality may reflect the ability of metabolically active tissues LOO - ,lipid peroxy radicals to repair themselves. Despite the unresolved questions regarding the biochemical origin of oxygen-induced injury, vitamin E has been administered to neonates in an attempt to protect against oxygen-induced tissue damage. Although the therapeutic expe- Modern neonatal care has improved the survival of low birth rience with vitamin E is now extensive, controversy continues weight infants. Paramount for the survival of the low birth weight regarding the appropriate indications and dosage for vitamin E infant is the use of increased oxygen concentrations to support therapy (8, 9). an immature cardiorespiratory system. However, the reduction This report presents the results of experiments designed to test in mortality has been associated with an increase in chronic the hypothesis that lipid peroxidation is increased by oxidative morbidities. Among these are several complications associated challenges in the newborn. Three experimental conditions were Received September 30, 1985; accepted January 24, 1986. utilized to explore the extent of lipid peroxidation in newborns. Address for correspondence and reprint requests Dr. Robert J. Roberts, M.D., The first experiments examined the effect of oxygen on biochem- Ph.D., Department of Pediatrics, University of Iowa Hospitals and Clinics, W-220 ical parameters of in vivo lipid peroxidation in newborn rabbits. GH, Iowa City, IA 52242. J.R.W. was supported by a Fellowship Award in Clinical Pharmacology from To further test the hypothesis that hyperoxic exposure increases the Pharmaceutical Manufacturers Association. in vivo lipid peroxidation, the antioxidant effectiveness of a- I Presented in part before the annual meeting of the Society for Pediatric tocopherol was examined in newborn rabbits exposed to room Research, Washington, D.C., May 1985. air or hyperoxia. The final series of experiments examined the Present address Division of Neonatology, Department of Pediatrics, University of Cincinnati Medical Center, 23 1 Bethesda Avenue, Cincinnati, OH 45267-054 1. parameters of lipid peroxidation after infusion of lipid emulsions Present address Division of Clinical Pharmacology and Ambulatory Pediatrics, while comparing the relative antioxidant effectiveness of a-to- Department of Pediatrics, University of Florida, Gainesville, FL 32603. copherol and a-tocopheryl acetate. The acetate ester of the 506 WISPE ET AL. naturally occurring isomer is the commercial form of vitamin E oil emulsion (Intralipid, lo%, Cutter Biological, Emeryville, CA). most commonly available. However, the esterified form is prob- Soybean oil emulsion was used because it contains approximately ably not active as an antioxidant until the acetate group is 5-10 mg/liter of a-tocopherol, compared to safflower oil emul- removed (10). In addition, the tissue disposition of intravenous sion which contains 25-30 mg/liter (13). Indwelling intravenous a-tocopheryl acetate is very different from that of a-tocopherol lines were placed, and a-tocopherol or a-tocopheryl acetate (100 (8). We compared these two forms of vitamin E in newborn mg/kg), or vehicle placebo (2 ml/kg) was given intravenously rabbits receiving lipid emulsion infusion, a clinically relevant immediately prior to lipid emulsion infusion. a-Tocopherol was situation in which lipid peroxidation is increased. administered as obtained from Hoffmann-LaRoche. As outlined above, the vehicle for the Hoffmann-LaRoche preparation dif- MATERIALS AND METHODS fers from other available parenteral preparations. Pure a-toco- pheryl acetate (Sigma Chemical, St. Louis, MO) was formulated The studies to investigate our objectives were conducted in in the same Emulphor 620 containing vehicle as the Hoffmann- three separate protocols. White New Zealand pregnant rabbits of LaRoche a-tocopherol. ,411 lipid infused animals received an known gestation, purchased from Morrison Rabbitry (West average dose of 3.7 g of lipid /kg, infused over 20 h. The pups Branch, 1.41, were delivered by cesearian section on day 31 of were studied for production of volatile hydrocarbons following gestation using 2.5% halothane in oxygen and local anesthesia completion of the lipid infusion. The animals were then killed, with 1% lidocaine. After delivery, the pups were placed in an and liver and lungs removed for determination of tissue TBA infant isolette (Air Shields, Inc., Hatboro, PA) with an air tem- reactants, tissue a-tocopherol and a-tocopheryl acetate concen- perature of 34" C. After a 1-h recovery period, the pups were trations, and tissue lipid peroxide content. weighed, marked, and one of three protocols instituted. None of Analysis of hydrocarbons. Hydrocarbons were analyzed using the PUPS in these studies received any enteral feeding%but all gas-liquid chromatography as previously described (14, 15). An- received twice daily parenteral fluids consisting of glucose and imals were placed in a 1 .4-liter glass-topped, stainless steel cham- electrolytes (1 m1/10 g body weight) by subcutaneous clysis. ber which was part of a closed, recirculating system. The atmos- Room air versus hyperoxia. The first Set of experiments was phere in the closed system was circulated continuously through designed to study the effects of hyperoxia (F102 >0.9) on lipid soda lime. Oxygen consumption was monitored by means of a peroxidation in the presence or absence of a-tocopherol. Imme- water manometer, and the oxygen consumed replaced with diately after delivery,
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