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Effects of Ductus Venosus Obstruction on Liver and Regional Blood Flows in the Fetal Lamb

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Effects of Ductus Venosus Obstruction on Liver and Regional Blood Flows in the Fetal Lamb 003 1-399819112904-0347$03.00/0 PEDIATRIC RESEARCH Vol. 29, No. 4, 1991 Copyright O 1991 lnternational Pediatric Research Foundation, Inc. f'rinlcd in U.S. A. Effects of Ductus Venosus Obstruction on Liver and Regional Blood Flows in the Fetal Lamb COLIN D. RUDOLPH, REBECKA L. MEYERS, RENE P. PAULICK, AND ABRAHAM M. RUDOLPH Cardiovascular Reseurch Institute and the Departments of Pediatrics, Surgery and Obstetrics, Gynecology, and Reproductive Sciences, University of California, Sari Francisco, Calfirnia 94143 ABSTRACr'. The ductus venosus allows highly oxygen- then drains into the inferior vena cava. Streaming patterns in ated blood returning from the umbilical-placental circula- the inferior vena cava and right atrium preferentially distribute tion to bypass the liver, and is believed thereby to facilitate the highly oxygenated blood that passes through the ductus preferential distribution of this blood to the fetal brain and venosus to the fetal brain and heart (1). During umbilical cord heart. To examine this hypothesis, we developed a model compression (2) and fetal hemorrhage (3), increasing proportions that allows acute obstruction of the ductus venosus in of the blood returning in the umbilical vein from the placenta chronically catheterized fetal lambs. In seven fetal lambs, pass through the ductus venosus. These observations have sug- a Swann-Ganz catheter was inserted into the inferior vena gested that the ductus venosus facilitates the preferential distri- cava and the balloon tip advanced into the ductus venosus. bution of highly oxygenated blood to the fetal brain and heart. Control measurements were obtained 1-2 d after surgery, However, the role of the ductus venosus is uncertain. The fetal before and during inflation of the balloon in the ductus foal, swine, and guinea pig lack a ductus venosus at term (4, 5). venosus. At each sample time, radioactive microspheres Previous studies in three late gestation, acutely exteriorized fetal were injected to determine organ blood flow and the distri- lambs have suggested that ductus venosus constriction has no bution of umbilical venous blood flow. During balloon effect on carotid arterial O2saturation or systemic blood pressure inflation, the percentage of umbilical venous return passing (6). through the ductus venosus was reduced from 38 2 15% To explore the role of the ductus venosus and to examine the to 1 f 0.5%. Umbilical-placental blood flow was unchanged hypothesis that the ductus venosus facilitates the preferential from control values of 181 f 33 mL/min/kg. Total liver distribution of highly oxygenated blood to the fetal brain and blood flow increased from 346 f 98 to 553 f 105 mL/min/ heart, we developed a model that permits intermittent ductus 100 g. Pressure in the inferior vena cava did not change, venosus obstruction in chronically catheterized fetal lambs. but umbilical venous pressure increased from 7.2 2 2.7 to Using this model, we examined the effect of acute ductus venosus 8.7 f 3.5 mm Hg. Total vascular resistance across the obstruction on oxygen and blood flow distribution to fetal organs liver and ductus venosus increased from 0.013 ? 0.006 to in normoxemic and hypoxemic fetal lambs. We also measured 0.020 2 0.011 during ductus venosus obstruction. Fetal alterations in hepatic vascular resistance and blood flow during heart rate, arterial blood pressure, and descending aortic ductus venosus obstruction. pH and blood gases were unchanged, as was oxygen content in the descending aorta and carotid artery. Organ blood MATERIALS AND METHODS flows, combined ventricular output, and oxygen delivery were also unchanged. In five animals, these studies were Animal preparation. Studies were approved by the Committee repeated during maternal hypoxemia. Similar changes in on Animal Research at the University of California, San Fran- liver blood flow were observed. Organ blood flows and cisco. Seven fetal lambs, 129 k 3 d gestational age (term, 147 d) oxygen delivery were not altered by ductus venosus ob- were fasted for 24 h before surgery. Epidural anesthesia was struction during hypoxemia. We conclude that obstruction achieved in the ewe with 2 mL of 1 % tetracaine hydrochloride. of the ductus venosus has no effect on regional blood flow Ketamine was administered i.v. to the ewe (100 mg bolus every distribution or oxygen delivery in normoxemic or hypox- 10-1 5 min) and intramuscularly to the fetus (5 mg/kg estimated emic animals. Because the hepatic microcirculation has fetal weight before thoracotomy) for sedation. Local anesthesia such a high compliance, the ductus venosus is not crucial with 0.25% lidocaine hydrochloride was used for all fetal inci- in regulating umbilical venous return to the central fetal sions. The ewe received a continuous infusion of 10% dextrose circulation. (Pediatr Res 29: 347-352, 1991) in 0.9% NaCl throughout the surgical procedure. Polyvinyl catheters were inserted into a maternal pedal artery and vein and advanced to the descending aorta and inferior vena cava, respectively. In the fetus, polyvinyl catheters were inserted into the descending aorta, inferior vena cava, and umbilical vein Up to 50% of the blood returning from the umbilical-placental as described previously (7). Briefly, a 3- to 4-cm incision was circulation passes through the ductus venosus in the fetal lamb. made in the uterine horn over a fetal hind limb, through which The rest of the blood passes through- the hepatic sinusoids and catheters were inserted into both fetal pedal arteries and veins Received September 26, 1990; accepted December 5, 1990. and advanced to the descending aorta -and inferior vena cava, Correspondence: Colin D. Rudolph, M.D., Ph.D., Division of Gastroenterology, respectively. One of the catheters inserted into the inferior vena ASB-4, Children's Hospital Medical Center, Elland and Bethesda Aves., Cincinnati. cava was advanced so that the tip was at the level of the Ohio 45229-2899. diaphragm. The amnion was then separated from the allantoic Supported by National Heart, Lung and Blood Institute Program Project Grant HL-24056 and a Deutsche Fonchungsgemeinschaft Research Fellowship (DFG Pa membrane to expose a large umbilical vein along the mesenteric 34211-1) awarded to R. P. and a National Research Service Award (Training Grant border of the uterus. A 3.5 multiple side hole catheter was NO. HL 071 92-12) awarded to R. L. M. introduced into a small tributary entering the vein and was 348 RUDOLPH ET AL. advanced 12-15 cm into one of the main umbilical veins. A were repeated. The ewe was returned to room air and the animal second catheter was introduced 5-7 cm into the same vein for was again allowed to recover for at least 1 h. As noted above, the injection of microspheres. An amniotic catheter was inserted, blood pressure, heart rate, pH and blood gases, and blood lactate and the uterine incision was sutured. all were unchanged from control values before continuing the The uterus was extracted further, and a second uterine incision study. Fetal hypoxemia was again induced and after 5 min the was made over the right chest of the fetus and the right front leg balloon tip of the Swann-Ganz catheter was inflated to obstruct was gently delivered through the incision. A catheter was inserted the ductus venosus. Samples were obtained and microspheres into the brachial artery and advanced into the brachiocephalic injected 10 min after balloon inflation. artery. The leg was returned into the uterus and the right chest The ewes were killed with an overdose of sodium pentobarbital of the fetus was exposed. The fetal lung was retracted through a followed by an i.v. injection of 10 mL saturated KC1 solution. right thoracotomy in the 8th intercostal space, exposing the The uterus and individual fetal organs were dissected and inferior vena cava and diaphragm as described previously (8). A weighed. All organs were placed in formalin, incinerated, and purse-string suture was placed in the inferior vena cava 0.5 cm ground into a coarse powder for counting in a gamma scintilla- cephalad to the entry of the diaphragmatic vein. The vessel wall tion counter. Using a multichannel (1024) pulse height analyzer was punctured in the center of the purse-string and a 4 F Swann- (Norland, Fort Atkinson, WI), the activity of each isotope in Ganz catheter (American Edwards, Irvine, CA) was advanced each organ was determined using a least-square analysis method 3.5 cm from the vessel wall into the ductus venosus. The catheter (10). position was verified by comparing the oxygen saturation in the Calculations. Upper and lower body organ blood flows were ductus venosus catheter with that in the umbilical vein. The fetal calculated from the inferior vena cava injection of microspheres incision was sutured. Before closure of the uterine incision, lost and carotid artery or descending aorta reference samples, respec- amniotic fluid was replaced with warm 0.9% NaCl solution. All tively, such that: catheters were tunneled through the skin to the ewe's flank. Catheter positions were ultimately verified by postmortem ex- amination. where Q = blood flow and cpm = counts per min of the injected After surgery, the ewes recovered for at least 24 h before studies isotope (9). Blood flows are expressed as mL/min/I 00 g or mL/ were performed; they received a standard diet of alfalfa pellets. min/kg fetal weight. Combined ventricular output was calculated All vascular catheters were flushed daily with heparin solution by summing all the organ flows obtained from the inferior vena (I mg/mL). Antibiotics (penicillin, 1 000 000 U, and kanamycin, cava injectate and withdrawal volumes. Lung flow and potential 400 mg) were administered i.v. and instilled into the amniotic superior vena cava flow across the foramen ovale were not cavity daily.
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