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 and 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 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 .

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

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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 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 , on the left side, traversing the (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

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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. 2, Fig. 3), which communicate one with another by cross-connections. A small number of spiral arteries, arising from this skein, penetrate the base of the placenta, marginal to the sub-placenta, and supply three or more short arterial stems in the chorio-allantoic placenta (PI. 2, Fig. 4). Each arterial stem derives its blood supply from at least one spiral artery. The branches which arise from the arterial stems proceed up towards the fetal surface of the placenta and out towards the periphery. They divide repeatedly (PL 2, Fig. 5) and the finest branches supply the placental labyrinth (Kaufmann, 1969). There are cross-connections at all levels, from the arterial stems down to very small branches. The probable functional significance of the abundant cross-connections in the placenta and in the skein of arteries beneath it is illustrated by the following observations. When contrast medium was injected by needle puncture into only one of the radial arteries supplying the placenta, the entire arterial network of the placenta was filled with the medium. Similarly, after silver-clip occlusion of all but one of the radial arteries to a placenta, as well as of most of the branches of this remaining vessel, contrast medium still entered the major portion of the placenta when injected through a catheter in the uterine artery. The venous drainage of the labyrinth is difficult to elucidate by angiographie techniques. Venous channels running superficially in the chorio-allantoic placenta (Panigel, 1959) can usually be identified in injected specimens (PL 3, Fig. 6). They drain into two semicircular vessels situated just beneath the junction between the chorio-allantoic placenta and the placental base. Each of these, in their turn, empty through a single vein that runs in the margin of the placental base, outside the sub-placenta (PL 3, Fig. 6). In the mesometrium, the veins draining each placenta and adjacent portions of the uterine wall communicate by cross-connections and fuse to form one or two wide vessels that empty into the ovarian vein (PL 3, Fig. 6). The latter vessel is widely dilated in pregnant animals and is the main path of venous drainage from the uterus. It communicates with the ipsilateral uterine vein

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access 406 JV*. Egund and A. M. Carter which is a vessel of small calibre (Text-fig. 2; PL 4, Fig. 9). We have never seen any evidence of a major communication with the contralateral ovarian vein. The left ovarian vein always joins the left renal vein, forming a common stem almost 1 cm long, which empties into the inferior vena cava (Text-fig. 2 ; PL 4, Fig. 9). On the right side, the ovarian vein enters the vena cava together

Text-fig. 2. Venous drainage of the guinea-pig uterus in late pregnancy. Stippled areas represent the placentae. The utero-ovarian veins (arrows 1 ) have a large capacity whilst the uterine veins proper (arrows 2) are relatively narrow. Observe that the left ovarian vein joins the left renal vein to form a common stem that drains into the vena cava.

EXPLANATION OF PLATES 1 AND 2 PLATE 1 Fig. 1. Angiography performed by selective catheterization of the right uterine artery from the right femoral artery in a pregnant guinea-pig, about 65 days post coitum. In this early arterial phase, the contrast medium has not yet reached the placenta, but the dilated radial arteries supplying it are well demonstrated (arrows). Fig. 2. Angiography performed by selective catheterization of the right ovarian artery from a carotid artery in a pregnant guinea-pig, about 58 days post coitum. Contrast medium is seen in the corpora lutea of the ovary (arrow) and in the most lateral of the two placentae which were situated in this uterine horn. PLATE 2 Fig. 3. Skein of meandering dilated arteries in the uterine wall beneath a guinea-pig placenta, about 61 days post coitum. Cross-connections between these vessels can be seen. The preparation was made by first injecting the uterus with barium sulphate suspension and then peeling the uterine wall away from the placenta. (The four markers are silver clips used at a previous stage of the preparation.) Fig. 4. Spiral arteries (arrows) leading from the skein of vessels in the uterine wall, past the sub-placenta to the chorioallantoic placenta in the guinea-pig. The preparation was made by injecting barium sulphate suspension into a single radial artery supplying two placentae in a pregnant uterus at about 46 days post coitum. Fig. 5. Angiography performed by selective injection of contrast medium in a uterine artery in a guinea-pig at about 63 days post coitum. The uterus had been exposed and two radial arteries occluded with silver clips. The contrast medium has entered two spiral arteries, one to each placenta, and is beginning to fill the arteries within the placentae, partly through anastomoses (white arrow-heads).

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access PLATE 1

(Facing p. 406)

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access PLATE 2

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access PLATE 3

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access PLATE 4

(Facing p. 407)

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access Placental vasculature of the guinea-pig 407 with the relatively short renal vein. The uterine veins invariably join the ipsi- lateral external iliac veins together with the internal iliac veins. Special attention was paid to the relationship between the arterial supply to the ovaries and the venous drainage of the uterus. Each ovary is usually supplied by two arteries arising from the arterial loop about 4-5 cm from the aorta. These divide into numerous small branches before entering the ovary. At least one branch follows the oviduct and anastomoses with arteries in the uterine wall. A relatively wide vein runs from the most lateral part of the uterine horn. Before joining the principal ovarian vein, this passes through the network of arteries supplying the ovary (PL 4, Fig. 10). The paired umbilical arteries, arising from the fetal iliac arteries, do not communicate until just before the point of their insertion in the placental disc. There they either fuse to form a short common stem or are joined by a short, transverse connection, subsequently branching over the upper surface of the placenta (PL 3, Fig. 7). Secondary branches dip down to the base of the pla¬ centa and divide throughout their length to supply the fetal placental capillaries. The pattern of branching of the veins is very similar to that of the arteries (PL 3, Fig. 8), each arterial branch being accompanied by a corresponding vein. The single empties into the left branch of the portal vein. The vitelline artery and the vitelline vein, deriving from the distal part of the superior mesenteric artery and vein, respectively, also run for a short distance in the umbilical cord before leaving to supply the inverted yolk sac placenta.

DISCUSSION Previous authors using arteriography to study the pharmacodynamics of maternal placental circulation in the guinea-pig (Bell & Brown, 1971; Girard,

EXPLANATION OF PLATES 3 AND 4 PLATE 3 Fig. 6. Venous drainage of a uterine horn, containing one placenta, of a pregnant guinea-pig at about 46 days post coitum. After the vessels had been injected with barium sulphate suspension and gelatin, most of the uterine tissue was cut away. Venous channels run superficially in the placenta to drain by two veins (arrows) marginal to the sub- placenta. Observe the many cross-connections between the veins in the mesometrium. Fig. 7. Guinea-pig feto-placental arteries, at about 58 days post coitum, demonstrated by injecting barium sulphate suspension into one of the umbilical arteries. Fig. 8. Feto-placental veins, in a guinea-pig placenta from the same uterus as the placenta shown in Fig. 7, demonstrated by retrograde injection of barium sulphate suspension into the umbilical vein. PLATE 4 Fig. 9. Retrograde phlebography performed by super-selective catheterization of the left ovarian vein from a jugular vein, in a guinea-pig, about 59 days post coitum. There were two placentae on this side. The tip of the catheter in the ovarian vein is indicated (circle), as are the left renal vein (arrow 1), the left uterine vein (arrow 2), and the left common (arrow 3). The last two vessels and the vena cava are filled by contrast medium draining in an antegrade direction. Fig. 10. Angiography performed by selective catheterization ofthe left ovarian artery from the right femoral artery in a guinea-pig. A prolonged injection of the contrast medium en¬ abled both the arterial and venous phases to be demonstrated. The ovarian artery (arrow 1) and ovarian vein (arrow 2) are indicated. A vein (arrow 3) from the tip of the uterine horn passes through the network of arteries supplying the ovary (arrow 4).

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access 408 . Egund and A. M. Carter Brun & Muffat-Joly, 1971) seem to have overlooked the dual arterial supply to the uterus and injected their contrast medium in the aorta caudal to the origin of the ovarian arteries. In the present paper, techniques of selective catheterization have been described which enable both the uterine and the ovarian arteries to be examined. The relative importance of these two vessels is difficult to determine with exactitude. In the renal vascular bed, there is a fair to good correlation between the cross-sectional area of the artery and the rate of blood flow (Ludin, Elke, Fehr & Thoelen, 1967; Göthlin, Hegedüs & Olin, 1973). If a similar relationship exists for the ovarian and uterine arteries in the present case then, on the basis of their calibres in the last fortnight of pregnancy, they should carry 25% and 75% of the blood flow, respectively. Moll & Künzel (1971) arrived at a figure of 60% for the uterine artery by a somewhat complex mathematical analysis of pressure measurements in the arterial loop and radial arteries; in a later paper, they express dissatisfaction with these measurements (Moll & Künzel, 1973). Schniewind & Asshauer (1962) claim that the uterine artery carries only 20% of the blood to each horn, yet present no evidence in support of this remarkable statement. It is general knowledge that the ovarian veins, sometimes called the utero- ovarian veins, carry the principal part of the venous drainage of the uterus; the intimation by Del Campo & Ginther (1972) that this circumstance may be altered in pregnancy should be disregarded. Endocrinologists frequently find cause to sample utero-ovarian venous blood (Blatchley, Donovan, Horton & Poyser, 1972), but a technique for atraumatic catheterization of the vessels from the jugular vein has not previously been described. In the rat, it has been shown that the ovarian venous blood flow decreases rapidly following direct cannulation (Piacsek & Huth, 1971). Schniewind & Asshauer (1962) state that the ovarian arteries of the guinea- pig join by mid-line anastomosis to form a continuous loop and that the ovarian veins behave likewise. They do not clearly define the relationship between the ovarian and uterine arteries or veins. Their interpretation has been quoted by subsequent authors using the guinea-pig placenta for double perfusion studies (Thomsen, Schniewind, Schultze-Mosgau, Krämer & Jost, 1966; Fischer, 1967), but finds no support in our observations. Although we have used several strains of guinea-pig, we have never seen a connection in the mesometrium between the major arteries or veins of the left and right uterine horns. Our findings are in accordance with those made in eight non-pregnant guinea-pigs by Del Campo & Ginther (1972) and with a brief description of the arterial loop given by Moll & Künzel (1971). The radial arteries pursue a devious route with many twists and turns from the arterial loop to the base of the placenta. A great deal of energy must be lost during passage of the blood through these vessels, entailing a fall in both lateral pressure (potential energy) and flow velocity (kinetic energy). Another notable feature of the radial arteries is their progressive increase in calibre. The increase in cross-sectional area will further accentuate the diminution of flow velocity but, in accordance with Bernouilli's principle (Folkow & Neil, 1971), somewhat counteract the decrease in lateral pressure. Moll & Künzel (1973) have verified that the net decrease in the mean blood pressure is con-

Downloaded from Bioscientifica.com at 10/10/2021 08:17:46PM via free access Placental vasculature of the guinea-pig 409 siderable and it is presumably accompanied by a dampening of the pulse amplitude. The overall effect will be a slow even perfusion of the placental labyrinth with blood at a fairly low pressure. A similar result is achieved in the uteroplacental circulation of the rabbit, rat, and man, although the morpho¬ logical arrangements are different (Carter, Göthlin & Olin, 1971). Presumably, therefore, these are the ideal haemodynamic conditions for effective placental exchange. The veins draining the gravid uterus are of such wide calibre that their resistance to flow must be very low and the pressure gradient between the placentae and the vena cava must be small. Again, there is a resemblance to the rabbit, in which the uterine veins are said to contain up to one-sixth of the total blood volume (Barcroft & Rothschild, 1932). The arterial and venous components of both placental circulations could be demonstrated in preparations injected with barium sulphate suspension. The exact relations between the maternal and fetal placental circulations can, however, be revealed only by histological and ultrastructural studies. It is apparent from the literature that the guinea-pig placenta is haemomonochorial, as is that ofman, but labyrinthine rather than vinous (Enders, 1965). Kaufmann (1969) claims that, in the placental labyrinth, maternal and fetal blood flow in opposite directions, and transplacental oxygen exchange certainly occurs with an efficiency suggestive of a modified countercurrent system (Bartels et al., 1967). It has been suggested as a mechanism for luteolysis in the guinea-pig that prostaglandin F2x secreted into the utero-ovarian vein may pass to the ovarian artery by countercurrent exchange (Blatchley et al., 1972). We cannot, however, agree that there is close contiguity between these main vessels. On the other hand, we have been able to confirm by angiography in vivo (PL 4, Fig. 10) that blood from the tip of the uterine horn drains through a vein which passes through the network ofarteries supplying the ovary, as was tentatively suggested by Del Campo & Ginther (1972). Neither our technique nor that of the latter authors has revealed any well-differentiated structure in this area, suggestive of an exchange system. When serial angiography is performed in vivo after selective catheterization of the ovarian and/or uterine artery, it is possible to follow the passage of contrast medium through the arteries, placental labyrinth ('capillary' phase) and veins. We are using this technique for pharmacoangiographic studies of the maternal placental circulation.

ACKNOWLEDGMENTS We are indebted to Dr Tord Olin for valuable advice and encouragement during the course of this study. The investigation was supported by the Swedish Medical Research Council (grant No. B74-14X-605-08A) and the Royal Physiographic Society of Lund.

REFERENCES Angantyr, L. G. & Olin, T. (1973) Description of a film changer for small animals. Ada radiai. Diagn. 14, 337.

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