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Chronic Partial Ureteral Obstruction in the Neonatal Guinea Pig. I

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Chronic Partial Ureteral Obstruction in the Neonatal Guinea Pig. I 1266 CHEVALIER AND KAISER 003 1-3998/84/18 12-1266$02.00/0 PEDIATRIC RESEARCH Vol. 18, No. 12, 1984 Copyright O 1984 International Pediatric Research Foundation, Inc. Printed in U.S.A. Chronic Partial Ureteral Obstruction in the Neonatal Guinea Pig. I. Influence of Uninephrectomy on ~rowthand Hemodynamics ROBERT L. CHEVALIER AND DONALD L. KAISER with the technical assistance of Anthony V. Broccoli Departments of Pediatrics and Internal Medicine, University of Virginia School of Medicine, Charlottesville, Virginia 22908 ABSTRAm. Although obstructive nephropathy is a fre- RBF renal blood flow quent cause of renal insufficiency in infancy, factors influ- BUN, blood urea nitrogen encing adaptation to chronic partial ureteral obstruction RVR renal vascular resistance (CPUO) are poorly understood. Guinea pigs were subjected RPF, renal plasma flow to unilateral CPUO within the first 2 days of life (Group Hct, hematocrit I) and microsphere studies were performed at 23 2 3 days AP, arterial pressure of age. To also investigate the role of functional renal mass on growth and hemodynamics, contralateral nephrectomy was performed in Group I1 at the time of ureteral constric- tion. Compared to sham-operated controls (ureteral diam- eter = 1 mm) CPUO caused impaired somatic growth in Obstruction of the urinary tract is an important cause of renal both groups. Resulting hydroureteronephrosiswas variable insuficiency in infancy (15). Complete ureteral obstruction in and most severe (ureteral diameter > 3 mm) in azotemic utero results in a nonfunctional kidney, often with severe dyspla- animals of Group 11, which demonstrated reduced compen- sia (6). However, congenital partial urinary tract obstruction satory renal hypertrophy and poorest somatic growth. often leads to progressive renal insuficiency which may in some Mean arterial blood pressure was not affected by CPUO cases be prevented or reversed by timely surgical correction (19). or uninephrectomy. Renal blood flow (RBF) was higher in Numerous studies have addressed the physiologic mechanisms Group I1 than Group I, and did not fall significantly with leading to decreased GFR during and following relief of complete severity of CPUO in Group 11, in which number of perfused ureteral obstruction, while relatively few investigations have been glomeruli was similar to controls. In contrast, renal vas- made of CPUO (20). Furthermore, as renal mass and hemody- cular resistance (RVR) increased by 172% in animals of namics are changing rapidly in the early postnatal period, CPUO Group I with severe CPUO, and was associated with 34% in the neonate may differ from that in the adult. The present fewer perfused glomeruli than in the hypertrophied contra- study was therefore designed to answer the following questions: lateral kidney. With increasing severity of CPUO, RBF 1) What is the effect of CPUO on postnatal renal and somatic tended to be distributed to outer cortical regions in the growth? 2) How are intrarenal hemodynamics altered by neo- obstructed kidney of Group I, while the shift in RBF natal CPUO? 3) How is the newborn kidney subjected to CPUO distribution was from outer to inner cortex in the remaining affected by reduced renal mass? kidney of Group 11. Filtration fraction fell as a result of The guinea pig was chosen as the species for'study because, as CPUO in both groups, such that reduction in the glomer- in the human, nephrogenesis is completed at birth and functional ular filtration rate was due in large part to factors other renal maturation proceeds during the first 4 postnatal weeks (2, than RBF. In conclusion, CPUO in the neonatal guinea pig 17). Unilateral partial ureteral obstruction was performed within causes marked alterations of glomerular perfusion. Contra- the first 2 days of life and animals were studied at 3 wk of age, lateral nephrectomy prevents the rise in RVR due to during the time of most rapid superficial nephron maturation. CPUO, possibly by preserving perfusion to all nephrons and shifting blood flow to more mature deeper cortical glomeruli. (Pediatr Res 18:1266-1271, 1984) MATERIALS AND METHODS Abbreviations Ninety-four Hartley guinea pigs (46 males and 48 females) were anesthetized with halothane within the first 48 h of life, and GFR glomerular filtration rate a midline abdominal incision was made in each animal. In 32 CPUO chronic partial ureteral obstruction guinea pigs (Group I) a 2-mm length of sterilized polyethylene tubing (PE50 or PE60, Clay Adams, Parsippany, NJ) was slit Received March 12, 1984; accepted May 22, 1984. longitudinally and placed around the distal third of the left ureter. Requests for reprints should be addressed to Robert L. Chevalier, M.D., De- partment of Pediatrics, Box 386, University of Virginia Medical School, Charlottes- To serve as controls, the ureter was left untouched in 16 addi- ville, Virginia, 22908. tional animals studied concurrently. In 31 guinea pigs (Group This work was supported by National Institutes of Health Grant 5 SO7 RR 11), polyethylene tubing was' placed around the left ureter as 0543 1-2 I, by a Grant-in-Aid from the American Heart Association, and with funds above, and the right kidney was excised after ligating the renal contributed in part by the American Heart Association, Virginia Afiliate. R.L.C. is an Established Investigator of the American Heart Association. Portions of this pedicle. Fifteen animals undergoing only right nephrectomy study were presented at the Annual Meeting of the Society for Pediatric Research. sewed as controls for this group. The incision was sutured in two San Francisco, CA, May 2, 1984. layers, and animals were returned to their mothers until weaning CHRONIC PARTIAL URETERAL OBSTRUCTION 1267 at 14 days. After 14 days, animals were fed standard guinea pig The kidney@) were decapsulated, bisected longitudinally, chow. Both males and females were pooled in eachgroup because weighed, and fixed in 10% formalin solution. Radioactivity of there is no difference in somatic or renal growth between sexes the blood sample and kidneys was measured in a gamma scintil- in the age range studied (1). Only animals with birth weight 75- lation counter (Beckman Instruments, Irvine, CA). One-half of 130 g were used, and litter size was reduced when necessary to a the kidney was digested in 25% hydrochloric acid and the num- maximum of four. ber of perfused glomeruli was determined as described previously Guinea pigs were fasted with free access to water the night (2). In the remaining half, five cores, 3 mm in diameter, were before study at 18-30 days of age. Animals were anesthetized punched out perpendicular to the surface of the kidney. Medul- with intraperitoneal sodium pentobarbital, 3 mg/100 g body lary tissue was cut away and the remaining cortex was divided weight and placed on a thermostatically controlled heating table into equal thirds (outer, middle, and inner) and slices from each to maintain rectal temperature at 39 * 0.5" C. Tracheostomy level were pooled for measurement of radioactivity as previously was performed and a jugular vein was cannulated for infusion of described (3). Remaining kidney tissue was weighed before and 0.9% saline at 0.3 m1/100 g body weight/h. In Group I, I3H] after drying at 40" C for 10 days for calculation of dry/wet ratio. inulin (New England Nuclear, Boston, MA) was added to the In four guinea pigs of Group I with severe ureteral obstruction, saline infusate in a concentration of 10 pCi/ml, while 100 pCi/ urine was withdrawn from the dilated ureter by sterile needle ml as added for Group 11. The contralateral jugular vein was puncture, plated on sheep blood and McConkey's agar, and cannulated for infusion of donor guinea pig plasma at a rate of incubated at 37" C for 48 h. 0.9 * 0.1 ml/h, adjusted to maintain constant Hct as described Calculations. Inulin clearance was calculated from standard previously (1). A polyethylene catheter was threaded down the formulas and filtration fraction was given by Ei,. RBF was right carotid artery such that the catheter tip lay at the aortic calculated from microsphere data using the relationship RBF = root. Mean AP was continuously recorded from this catheter by K.q/b, where K = radioactivity of whole kidney, q = withdrawal means of a Statham 231D pressure transducer coupled to a rate of aortic blood reference sample, and b = radioactivity of Hewlett-Packard 7754B recorder. reference blood sample. RPF was calculated as RPF = RBF (1 The abdominal contents were exposed through midline and - Hct), and GFR as GFR = RPF. Ein.RVR was calculated as left subcostal incisions, and the left kidney was covered with RVR = (AP - RVP)/RBF, where RVP = renal venous pressure, saline-soaked cotton (Group I) or placed in a Lucite cup and assigned a value of 3.5 mm Hg (3). bathed in saline maintained at 39 f 0.5" C (Group 11). Ureteral Statistical analysis. Data were evaluated by two-way analysis diameter was constant proximal to the obstruction, and external of variance and Duncan's multiple range test using the Statistical diameter was measured halfway between kidney and bladder Analysis System (S. A. S. Institute, Inc., Cary, NC). The effects using calipers under microscopic visualization. A polyethylene of ureteral obstruction and of contralateral nephrectomy were catheter was inserted in the abdominal aorta at the aortic bifur- examined separately, and interaction between these variables was cation and connected to a second pressure transducer. A flared also examined. As birth weight was lower in Group I1 than polyethylene cannula was sutured into the bladder for collection Group I, and experimental body weight in control animals is of urine. To minimize dead space, bladder volume was reduced dependent on birth weight (R = 0.81, p < 0.001), analysis of by pulling the anterior bladder wall through the ligature around covariance was also camed out for body weight and kidney the cannula.
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