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The Vascular Anatomy of the Ovary and the Relative Contribution of the Ovarian and Uterine Arteries to the Blood Supply of the Ovary in the Guinea-Pig M

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The Vascular Anatomy of the Ovary and the Relative Contribution of the Ovarian and Uterine Arteries to the Blood Supply of the Ovary in the Guinea-Pig M J. Anat. (1983), 137, 3, pp. 457-466 457 With 7 figures Printed in Great Britain The vascular anatomy of the ovary and the relative contribution of the ovarian and uterine arteries to the blood supply of the ovary in the guinea-pig M. I. HOSSAIN* AND J. D. O'SHEAt * Department ofAnatomy and Histology, Bangladesh Agricultural University, Mymensingh, Bangladesh and t Department of Veterinary Preclinical Sciences, University ofMelbourne, Parkville, Victoria, Australia 3052 (Accepted 13 January 1983) INTRODUCTION The mammalian ovary derives its main arterial supply from the ovarian artery which arises from the abdominal aorta or from the renal artery (Mossman & Duke, 1973; Reynolds, 1973). The blood vessels supplying and draining the ovaries of the guinea-pig have been described briefly (Potter, Jones & Hermann, 1958; Shively & Stump, 1975; Cooper & Schiller, 1975), although DelCampo & Ginther (1972) have given a detailed account of the anatomy of the extrinsic ovarian vasculature and have related it to the presence of a unilateral luteolytic mechanism in this species. There are no published data on the intrinsic vasculature of the ovary of the guinea-pig. However, it has been reported that the intrinsic vasculature of the ovary differs widely both between species and during different functional states (Clark, 1900; Burr & Davies, 1951; Delson, Lubin & Reynolds, 1948; Delson, Lubin, Brooklyn & Reynolds, 1949; Reynolds, 1973). In most mammals, there are anastomoses between branches of the ovarian and uterine arteries (Mossman & Duke, 1973; Reynolds, 1973). In relation to their potential contribution to ovarian blood supply, it is clearly important to know the direction of blood flow in these anastomoses. The simplest approach is to compare the diameters of the various vessels. On this basis, it has been concluded that flow in these anastomoses is probably towards the uterus in the horse, sheep and pig (DelCampo & Ginther, 1973), and towards the ovary in the rat, hamster, guinea-pig (DelCampo & Ginther, 1972), rhesus monkey (Ginther, Dierschke, Walsh & Del- Campo, 1974) and, on the side ipsilateral to the corpus luteum, in the ox (Ginther & DelCampo, 1974). However, in a later study in which microspheres labelled with different isotopes were injected into the left ventricle, and into the aorta between the origins of the ovarian and iliac arteries, Chaichareon, Rankin & Ginther (1976) have concluded that the flow in this anastomosis is towards the uterus in the guinea-pig. In view of such contradictory results, further investigation, using different methodology, has been considered worthwhile. This paper reports a study of the extrinsic and intrinsic vasculature of the ovary in the guinea-pig, and of the direction of blood flow along the arterial anastomosis between the uterine and ovarian arteries. 458 M. 1. HOSSAIN AND J. D. O'SHEA RK R CL L$O~VV E ARC OBAD RA L OVA Fig. 1. Diagrammatic representation of the ventral view of the arteries supplying, and the major veins draining, the ovary of the guinea-pig. AO, aorta; VC, vena cava; AD RA, additional renal artery; 0 V B A D RA, ovarian branch of additional renal artery; R 0 V, right ovary; CL, corpus luteum; E ARC, extra-ovarian arterial arcade; R 0 V V, right ovarian vein; L 0 V V, left ovarian vein; L O VA, left ovarian artery; L R V, left renal vein; RK, right kidney. Arrow indicates the region where direction of blood flow was observed. MATERIALS AND METHODS Animals Adult female Dunkin-Hartley guinea-pigs were used in these studies. Timing of the stages of the oestrous cycle was based on daily observation for vaginal opening; vaginal smears were taken on days when the vagina was open. The first day of com- plete vaginal opening when the smear contained abundant comified epithelial cells, with very few nucleated epithelial cells or leucocytes, was designated Day 1 of the cycle. In all the animals, at least two consecutive oestrous cycles of 15-19 days had been observed immediately preceding the cycle in which the experiment was conducted. Ovarian vasculature Latex studies were carried out on fifteen animals between Days 6 and 12 of the cycle. Latex was injected either into the arterial system or venous system or both. Latex of two contrasting colours was used when both systems were injected. Specimens were fixed by immersion in a solution containing 30 % of 95 % ethanol, 10 % formalin, 10 % glacial acetic acid and 50 % distilled water (DelCampo & Ginther, 1972) for 48-72 hours. They were then studied with a dissecting microscope after either dissection, clearing in benzene and benz> benzoate (Orsini, 1962; DelCampo & Ginther, 1972) or maceration for 48 ho rs in 20% sodium hydroxide at 50 'C. Two other methods were each used on a single animal on Day 10 of the oestrous Vascular anatomy of ovary in guinea-pig 459 OVA Fig. 2. Diagrammatic representation of the arteries to the ovary and corpora lutea of the guinea-pig. OV, ovary; OVA, ovarian artery (here ovarian branches of the ovarian artery); LA, luteal artery; CL, corpus luteum; I ARC, intra-ovarian arterial arcade. cycle. A silicon rubber cast was formed by injecting silicon rubber (Microfil, MV-1 12, Canton Biochemical Products, Inc., Boulder Co.) via the thoracic aorta. The injected specimen was fixed in 10 % formalin, dehydrated in alcohol and cleared using methyl salicylate. In the other method, a 2 % Berlin blue solution was injected via the aortic cannula. The reproductive tract, together with its attached ligaments, the contiguous peritoneal tissues, kidneys and aorta was dissected out as a single unit, pinned flat on a cardboard sheet, and fixed in 10 % formalin. The specimen was then cleared in dimethyl sulphoxide (Analar, BDH Chemical Ltd., Poole, England) for a week before examination. Direction ofbloodflow in utero-ovarian arterial anastomosis Six female guinea-pigs weighing 500-550 g, two animals each on Days 10, 12, and 16 of the cycle, were included in this experiment. The method was based on that described by O'Shea & Lee (1974) in the rat. The animals were fed on a restricted diet, with water ad libitum, so that weight remained almost constant over a period of 35 days, thereby reducing the amount of fat present in the broad ligament and around the ovarian and uterine vessels. Under either urethane or rentobarbitone anaesthesia (three animals, one each on Days 10, 12, and 16 of the cycle, were anaesthetised with each anaesthetic), the right common carotid artery was cannula- ted and the cannula was advanced to the left ventricle. The abdominal cavity was then opened with a mid-ventral incision, and the viscera carefully retracted to one side to expose the region of anastomosis between the ovarian and uterine arteries. The region was then -viewed under a dissecting microscope, care being taken to avoid touching the vessels. Since only small amounts of fat were present, the anastomotic vessels were clearly visible. Approximately 0-15 ml of a 2-5 % solution of Lissamine green, adjusted to pH 7*4 with 0 1 M sodium hydroxide solution, was 460 M. I. HOSSAIN AND J. D. O'SHEA ov ov V Fig. 3. Diagrammatic representation of the veins to the ovary and corpora lutea of the guinea- pig. CV, ovary; OV V, ovarian vein (here ovarian tributary of ovarian vein); LV, luteal vein; CL, corpus luteum. then injected via the carotid catheter from a 1 ml tuberculin syringe. The artery in the region of anastomosis was viewed simultaneously under a dissecting microscope to observe the direction of flow of the injected dye. Several repeated injections were made in all animals. The above procedure was performed on both left and right sides of all the animals studied. RESULTS Extrinsic ovarian blood vessels Arterial supply The ovaries were supplied by the paired ovarian arteries (Figs. 1, 4, 5). These arteries originated either from the aorta at about the level of origin of the renal arteries, or as branches of renal arteries, or by common trunks with renal arteries (Fig. 1). From their origins, the ovarian arteries passed caudally and laterally around the caudal poles of the kidneys (Figs. 1, 4, 5). These arteries were in close apposition to the corresponding veins on each side (Figs. 1, 6), supplied small branches to the tissues of the mesovarium and to the perirenal fat, and in some cases formed anastomoses with branches of the renal arteries. Each ovarian artery then gave rise to two or three ovarian and tubal branches, after which the main trunk ran more caudally to form a major end-to-end anasto- mosis with the cranial end of the uterine artery, so completing a closed loop with this vessel (Fig. 4). The ovarian and tubal branches formed spiralling coils around their longitudinal axis as they approached the ovary. Before reaching the hilus of the ovary, further branching took place from these ovarian and tubal branches, pro- ducing a total of 5- or 6 small, tightly coiled branches. Anastomoses between these Vascular anatomy ofovary in guinea-pig 461 Fig. 4. Ventral view of partially cleared Berlin blue injected arteries to the female genital tract ofthe guinea-pig. 0 V, ovary; O V A, ovarian artery; UA, uterine artery; K, kidney; 0 VB O V A, ovarian branches of ovarian artery. Arrow indicates the regions where direction of blood flow was observed. x 1-4. arteries were observed in the pedicle. The most caudal of the arteries supplied the uterine tube, infundibulum and mesosalpinx, and formed anastomoses (a) caudally with a branch or branches of the uterine artery on the tubal wall and (b) cranially with a branch or branches of one of the ovarian arteries coming around the cranial pole of the ovary, to form an extra-ovarian arterial arcade (Fig.
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