UTERINE AND PLACENTAL CIRCULATION IN THE GUINEA-PIG: AN ANGIOGRAPHIC STUDY N. EGUND and A. M. CARTER *Department of Diagnostic Radiology, University Hospital, Lund, and Institute of zloophysiology, University of Lund, Sweden {Received 8th February 1974) Summary. The distribution of arteries and veins to the uterine and maternal placental vascular beds of the guinea-pig was studied in vivo by serial angiography and post mortem by the injection of barium sulphate suspension. The main features of the fetal placental vessels were also demonstrated. There is a dual arterial supply to each uterine horn, the uterine and ovarian arteries joining to form a continuous loop. The radial arteries which arise from the arterial loop and supply the placentae pursue a meandering course and are widely dilated. The haemodynamic implication of this configuration is that the placentae are evenly perfused with blood at a low flow velocity and a relatively low mean pressure. The veins draining the uterus are of wide calibre, presenting little resistance to flow and allowing for a small pressure gradient between the placentae and the vena cava. Veins leaving the lateral part of the uterine horn pass through the network of arteries supplying the ovary, but no special arrangement for countercurrent exchange could be demonstrated. Techniques are described for the selective catheteriza- tion of the uterine and ovarian arteries and for super-selective catheteri- zation of the utero-ovarian veins from a jugular vein. INTRODUCTION The guinea-pig resembles man in having a discoid haemochorial placenta and has therefore been used in physiological studies of placental function (Bartels, El Yassin & Reinhardt, 1967; Fischer, 1967; Kiinzel & Moll, 1972). It seemed that this species might also be suitable for pharmacoangiographic studies of the maternal placental circulation, similar to those performed in the rabbit (Carter & Olin, 1972, 1973). We have therefore attempted, in the con¬ text of a wider survey (N. Egund & T. Olin, in preparation), to describe the roentgen anatomy of the uterine and placental vasculature of the guinea-pig and have developed techniques for selective catheterization of the ovarian and uterine arteries and of the utero-ovarian veins. Address for correspondence : Dr A. M. Carter, Institute of Zoophysiology, Helgonavägen 3 B> S-223 62 Lund, Sweden. 401 Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access 402 . Egund and A. M. Carter MATERIALS AND METHODS Thirty-eight pregnant guinea-pigs were used in this study. The stage of gesta¬ tion, estimated from the weight of the fetuses (Draper, 1920; Ibsen, 1928), varied from 35 to 65 days post coitum but in most animals was greater than 50 days post coitum. We also studied one animal soon after parturition and a number of non-pregnant females. General anaesthesia was obtained with intraperitoneal sodium pentobarbitone (Mebumalnatrium, ACO, Sweden) in an initial dose of 30 mg/kg body weight. A thin radiopaque polyethylene catheter was used for arteriography (OPP 10, Portex, England, o.d./i.d. = 0-65/0-25 mm). The tip ofthe catheter was tapered by pulling it in hot air to an outer diameter of 0-3 mm and the tip portion was moulded to form a hook. The radiopaque polyvinyl catheter used for phleb- ography (R/I/85, Portex, England, o.d./i.d. = 1-5/0-75 mm) was also tapered and slightly bent. The catheters were inserted by a cut-down technique, using a thin guidewire of stainless steel to stabilize the catheter. Catheterization was performed during magnification fluoroscopy using a roentgen tube with an 0-1x0-1 mm focal spot. The contrast medium employed was meglumine metrizoate (Isopaque Cerebral, Nyegaard A/S, Norway). The catheter for arteriography was inserted by way of a femoral artery or a common carotid artery and its tip was introduced into an ovarian, renal or internal iliac artery. The catheter for retrograde phlebography was inserted by way of a jugular vein and introduced super-selectively into the ovarian vein, on the left side, traversing the renal vein (see the anatomical description below). In a few animals, the uterus was exposed and the arteries supplying the placenta were successively occluded with silver clips to aid the study of the collateral circulation. We also exposed the fetuses by Caesarean section, punctured the umbilical vessels with a lymphography needle (lymphangio- graphy set No. 0-4, A/S Surgimed, Denmark) and injected small amounts of contrast medium to study the fetal placental circulation. Serial angiograms with twofold or fourfold geometric magnification, FFD 90 cm, were obtained using an automatic film changer (Siemens-Elema AB) with high definition screens. In the arterial occlusion experiments, we used a film changer for 9x12 cm industrial film (Structurix D4, Agfa Gevaert) immediately beneath the animal, FFD 45 cm (Angantyr & Olin, 1973). In post-mortem studies, the vessels were rinsed with isotonic saline solution and filled with barium sulphate suspension (Micropaque, Damancy Ltd, England). Dissections were then made to study the arrangement of arteries and veins in the maternal uteroplacental circulation and the fetal placental circulation. Documentation was secured on industrial film (Structurix D4 or D7, Agfa Gevaert). RESULTS The guinea-pig uterus is bicornuate and each horn receives its blood supply from an arterial loop formed by the anastomosis of the uterine artery with the Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access Placental vasculature of the guinea-pig 403 ipsilateral ovarian artery (Text-fig. 1). There are no significant anastomoses between this loop and the corresponding loop on the contralateral side. In the non-pregnant animal, the ovarian and uterine arteries have about the same calibre. During pregnancy, however, the uterine artery comes to predominate: towards the end of gestation, the calibre of the ovarian artery at its origin is about 0-7 mm and that of the uterine artery about 1-2 mm. The uterine artery on both sides arises from the internal iliac artery about 0-5 cm after its origin and is its first major branch. The ovarian arteries arise from the aorta at about the same level as the renal arteries (i.e. between the caudal part of the thirteenth thoracic vertebra and the middle of the first lumbar vertebra), which may be single or dual for each kidney. Occasionally, the right ovarian artery shares a common stem with a renal artery. Text-fig. 1. Arterial supply to the guinea-pig uterus in late pregnancy. The dotted line follows the outline of the uterus, the stippled areas represent the placentae and the two circles indicate the location of the ovaries. The ovarian artery (arrow 1 ), which on the right side arises with a renal artery, joins the uterine artery (arrow 2) to form a con¬ tinuous loop. Of the radial arteries arising from this loop, only those supplying the placentae are dilated (example indicated by arrow 3). There is a network of fine, anastomosing arteries in the uterine wall but no major connection between the arteries of the right and left uterine horns. The uterus is supplied by arteries which arise in a radial fashion from the utero-ovarian arterial loop, run for 1 to 3 cm in the mesometrium, and branch and anastomose freely in the uterine wall (Text-fig. 1). In the pregnant animal, a number of these radial arteries also supply the placentae. They are easily Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access 404 . Egund and A. M. Carter |b 3-S « S — co O t-* CO CO '— co — cp in — o o O CM CSI O - CM O O ¡ « CM — — — µ — — cm - co esco eô • cô cô — co r-- « s «§ I ^ OCO I C001OC0OC0 O O CO O CM CM dì en -~ — -> g G ì; — ò ô — — — — — — 4|| + r-~ to co r- ID - ID in m in t^. cor-.inm (9 -S c K »s feo •c lis t— c — O CO IO co in in in 8 ~ .2 t— CM· cp ^ ^ cp r^-tpinin . — — ? I — ò — — ¿ £ ü febS-S «· 5 s«^ J^B S* teC -s * * Iff "la S — — cm co en- - m m — — CM CM CO CO " — — — cm co ^.-- m Pipici hWhlJhU Pi Pi Pi Pi -l„--I-l ¡SÄ »il lì fis 1 ai 3 Sia s I Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access Placental vasculature of the guinea-pig 405 recognized by their wide calibre (PI. 1, Fig. 1), which increases progressively from their origin to their arrival at the placental site (Table 1), and by the tortuous course which they pursue in the mesometrium and uterine wall. There are one to three such arteries to each placenta. Occasionally, one artery divides to supply two or three placentae. Contrast medium injected into the uterine artery in vivo, at a rate approximating to the rate of blood flow, never reached the ovary (PL 1, Fig. 1) and sometimes failed to enter the most lateral of several placentae. Contrast medium injected at a physiological rate into the ovarian artery filled the ovary and several of the radial arteries. Thus, when the medium was injected by this route, it entered the most lateral of several placentae (PI. 1, Fig. 2) and usually reached a solitary placenta. The guinea-pig placenta is one ofthe most specialized found among the rodents. Its structure has been described in detail by Davies, Dempsey & Amoroso (1961), Müller & Fischer (1967) and Kaufmann (1969). The chorio-allantoic placenta is discoid and in the last third of pregnancy it rests on a base, usually smaller in diameter, in the centre of which is the sub-placenta. In the decidua beneath each placenta, the branches of the radial arteries build a skein of dilated meandering vessels (PI.