Okajimas Folia Anat. Jpn.. 69(1): 1-10, May, 1992

A Macroscopical Study of the Inferior Phrenic Artery of Female Rats, with Reference to the Embryological Background of Occurrence of the Genital Artery from this Artery

By

Shigeki MIZUKAMI, Shigenori TANAKA and Madoka MORIYA

School of Nursing, Fukui Prefectural College, Oohatamachi 97-21-3, Fukui 910 Department of Anatomy, School of Medicine, Kanazawa University, Takaramachi 13-1, Kanazawa 920

-Received for Publication, December 24, 1991-

Key Words: Inferior phrenic artery, Diaphragm, Genital branch. Pleuroperitoneal fold, Female rat

Summary: The principal aim of this study was to elucidate the general features of the inferior phrenic artery (IPA) of female rats which retain the original embryonic configuration of this artery. The artery of the right side was found to be detached from the renal artery, while that of the left side arose from the aorta. Between these fellow arteries, however, no essential morphological differences were discernible. At some point not far from their origin, they were found to break up into the ascending, suprarenal, suprareno genital and descending arteries. The ascending artery of the right side coursed along with the phrenic nerve, and vascularized a greatest portion of the total area of the partes sternalis et costalis of the diaphragm. Furthermore, the artery was found to be intimately associated with the inferior caval vein. Thus, it could be assumed that this artery of adult rats has been embryologically related to the musculus diaphragmaticus, transverse septum, ventral pleuroperitoneal fold, and the caval venous mesentery. The suprarenal artery took its course along the superior margin of this gland to reach the lateroinferior part of the pars costalis of the diaphragm. Its course and destination strongly indicates that in its development the suprarenal artery has been intimately related to the formation of the ventral pleuroperitoneal fold. The suprarenogenital artery was characterized as giving off a genital branch which entered first the diaphragmogenital ligament, and then took a descending course toward the ovary, in a quite similar manner of origin and course to those of the aberrant gonadal (testicular and gonadal) arteries observed in Japanese human adults (Shinohara et al., 1990; Hanie, to be published). The descending artery was observed to be closely associated with the major splanclinic nerve and the celiac ganglion. The variability of arteries of the IPA of female rats and also of humans, seems to reflect dramatic changes which have occured in the early stages of development, and have influenced more or less the morphology of the uppermost abdominal anlages of the followings: transverse septum, musculus diaphragmaticus, dorsal and ventral pleuroperitoneal folds, suprarenal gland and celiac ganglion, urogenital organs, inferior caval vein in the caval venous mesentery. In conclusion, it could be said that the anatomy of female rats provide us valuable clues as to the essential configuration of the IPA of humans and the relationships of the IPA to structures which are thought to be directly involved in the development of this artery.

The inferior phrenic artery (IPA) of human surrounding mesoderm both cause the gonads and beings is known to be distributed far more extensively the mesonephric tracts to descend from the initial than its name implies; this artery gives off branches location immediately below the diaphragm (Arey, not only to the diaphragm, but also to the suprarenal 1966; Patten, 1946); In the male, the testis courses gland, the celiac ganglion, the adiposal capsule of as far downward as the inguinal ligament by the the kidney, and to the inferior caval vein (Williams beginning of the third month and attains its final et al. 1989). This fact leads us to a supposition that position in the scrotum early in the ninth lunar the IPA's potential to supply blood to broad areas month (Arey, 1966). In the female, the ovary descends might be attributable to embryological situations in the same manner as the testis does. and reaches a under which the IPA of human embryos develops. point just inferior to the pelvic brim by the twelfth In this development the most substantially involved week of gestation (Moore, 1982). It is this descent of are the mesonephroi with the meso- or parameso- the gonads that renders it difficult for us to discern nephric ductus and the mesonephric ductuli; The with certainty the intimacy of the human IPA with progressive degeneration of mesonephroi and the the gonads and genital tracts in the anatomy of

Correspondence should be addressed to: Prof. Shigcki Mizukami. School of Nursing. Fukui Prefectural College. 0ohatainachi 47-21-3 Fukui Japan 910.

1 2 S. Mizukamiet al. human adults, although this artery has been reported solution at 60 C° for 3 days to make casts of the to occasionally give origin to the testicular artery blood vessels. (Shinohara et al., 1990) or give off an aberrant 2) Four rats, after the initial perfusion with 200 ml branch toward the ovary (Horie, to be published). of normal saline containing heparin, were perfused In contrast to human beings, the female adult rats with an additional 20 ml of normal saline containing concerned with in this study fortunately provide ca. 1% of coloring matter (Sakura Poster color/ us good research material, because in this animal Japan), and finally with 40 ml of 10% (v/v) formalin the ovary and the ovarian tube are closely associ- solution also containing ca. 1 percent of the coloring ated with the diaphragm, being connected by the matter; the animals so perfused were postfixed in the diaphragmogonadal ligament to the latter. This same fixative for 2-3 days. After the fixation, the topography of the ovary of the full-grown female rat abdominal wall, together with the abdomnal viscera is almost the same as that of the embryo of this including the adrenal glands, the ovaries and the animal. Therefore, it could be said that the ovary uterine tubes, and branches of the IPA, were resected and the genital tracts of female rats retain the position out, dehydrated in graded series of ethyl alcohol, nearest to the diaphragm as observed in early stages and cleared in xylene for examination. This pro- of rat embryos (Ganotte, 1984), and that this animal cedure allowed us a substantially improved investig- provides for us quite beneficial anatomical findings ation of the fine branches of the IPA. to discern the essential relationship of the IPA to the The observations of the anatomical details of transverse septum, the musculus diaphragmaticus, the IPA were performed exclusively under a ster- the dorsal and ventral pleuroperiotoneal folds, the eomicroscope at a maginfication of between 4 and suprarenal gland, the celiac ganglion, the gonad, the 10 times. The working field was illuminated by mesonephroi and the inferior caval vein, all of which two fiber optical goose neck lamps (Nikon). In are known to be importantly involved in the devel- the intervals between observations, the materials, opment of the IPA. To our knowledge, however, when required, were photographed on Neopan SS the morphological features of the IPA of rats are far (6.2 x 8.8 cm2) films with a camera (Mamiya RB67), from having entirely elucidated, and in the literature and enlarged on projection paper (Hishicopy/ very little information is available. The present study Mitsubishi; 42.0 x 59.3 cm2) to about 5-6 times was therefore undertaken to provide a detailed the actual size, where each finding was noted. The description of the overall features of the IPA of findings in this study are based on the data recorded female rats in the hopes of obtaining clues for a on a total of 10 photoprojection papers. better understanding not only of the IPA of female rats, but also of human beings as well. Findings Materials and Methods The morphology of the paired IPA was found in For the purpose of this investigation, 6 Wistar principle to be the same for both. Therefore, for the female rats (weighing between 150-300 gm) were sake of simplicity, the following accounts will be used; the animals were anesthetized first with ether, given primarily for the right side, whilst descriptions and then with intraperitoneally injected solution of the left IPA will be confined to describing essential of urethane (sodium ethylcarbamate, 900 mg/kg). differences from the right side. When the rats were completely narcotized, the thoracic cavity was opened and the heart exposed The IPA of the right side. for cutting open the left ventricle, through which a The IPA of the right side was found to issue from catheter was retrogradely inserted into the ascending the right renal artery on its way to the renal porta, aorta. Perfusion was commenced with 200 ml of and to course in the subperitoneal areolar tissue normal saline containing heparin (10 IU/ml). Out- which covers the inferior (or abdominal) aspect of flow of perfusate was from the cut right auricle. the diaphragm (Figs. 1 and 2). At some point not far When the ouflow was quite free of blood, the rats from the origin of this artery, the IPA split into the were divided into two groups and posttreated in the following arteries: (1) the ascending artery; (2) the following way: suprarenal artery; (3) the suprarenogenital artery; and (4) the descending artery. The description of 1) In two rats, 30 ml of neoprene latex (Showadenko- these arteries follows. Dupon) was injected. The rats so injected were immersed for 3 hours in a 1% aqueous solution of Ascending artery periodide acid, allowing the neoprene latex injected The ascending artery was seen arising as the direct into blood vessels to harden. The rats were thereafter continuation of the IPA and played a role in vascu- subjected to digestion by a 1% protease aqueous Thc Inferior Phrenic Artery of Female Rats 3

larizing the greatest portion of the diaphragm — i.e., the pars costalis of the diaphragm, and inferiorly to pars sternalis and pars costalis of the diaphragm, the ovary and the uterine tube. The superior genital excepting for the lateroinferior portion of the latter. branch was observed to descend in this ligament to (This portion was supplied by the suprarenal artery become contiguous with branches of the ovarian of the IPA as described below.) The ascending artery artery. A capsular branch was found branching off coursed upwards and slightly laterally in front of the from the superior genital branch en route to the medial lumbar crus of the diaphragm, accompanying diaphragmogenital ligament where it entered the the third branch of the phrenic nerve (see Laskowski substance of the adipose capsule of the kidney. Sanes, 1987). In regard to its topographical re- lationships with adjacent organs and vessels, the Descending artery ascending artery coursed close to the medial border The descending artery, being located laterally to of the kidney and the suprarenal gland. Furthermore, the principal trunk of the IPA, took downward and importantly, above the level of the suprarenal course on the lateral lumbar crus of the diaphragm gland, the ascending artery coursed in the caval (Fig. 2). This artery was found to accompany the venous mesentery, being located dorsal to this vein major splanchnic nerve as far downwards as the (Fig. 2). When the artery reached the caval foramen region where the celiac ganglion was located (not of the diaphragm, it was found to come together depicted). While taking this downward course, the with branches of the pericardiacophrenic artery of descending artery issued the suprarenogenital branch the internal thoracic artery which, after issuing from (not artery) which passed laterally across the dorsal the subclavian artery, coursed down, accompanying aspect of the kidney (Figs. 1 and 2). When reaching the phrenic nerve in the thorax cave to reach this the lateral margin of the suprarenal gland, it gave foramen. Here, the ascending artery was reinforced origin to a branch, the inferior suprarenal ramusculus by receiving an additional blood supply from the destined for the region around the lateroniferior pericardiacophrenic artery, and traversed through horn of the adrenal gland (Fig. 2). After emitting the substance of the superior and the laterosuperior the inferior suprarenal ramusculus, the inferior portions of the partes sternalis et costalis of the suprarenogenital branch finally gave rise to the inferior diaphragm, accompanying the first and second genital branch, which continued laterally and in- branches of the phrenic nerve (Laskowski & Sanes, feriorly, and reached the diaphragmogenital ligament, 1987). descending in this ligament to become contiguous with branches of the ovarian artery which ascended Suprarenal artery in this ligament (Fig. 2). The suprarenal artery coursed laterally along the superior margin of the suprarenal gland, giving off The IPA of the left side. numerous small branches — the superior suprarenal As described above, the essential features of the ramusculi to the upper part of this gland (Fig. 2). IPA of the left side were found to be of almost the Taking its course further laterally, the artery reached same configuration as that of the right side. Worthy' the lateroinferior portion of the partes sternalis et of note are the following differences: 1) that the costalis of the diaphragm just above the attachment principal portion of the left IPA, unlike that of the of the diaphragmogonadal ligament, and ended here right, was divided into two trunks, both arising from by dividing up into fine branches. the aorta, and not from the renal artery; one of the trunks gave common origin to the ascending and Suprarenogenital artery descending arteries, while the other gave rise to The suprarenogenital artery was found arising the suprarenal and suprarenogenital arteries, res- from the principal portion of the IPA, and coursing pectively, and 2) that the ascending artery has laterally to the dorsal aspect of the suprarenal gland nothing to do with the inferior caval vein, and just as (Fig. 1); here, it split up into numerous fine branches, in humans, rats are devoid of an inferior caval vein the middle suprarenal ramusculi which were dis- on the left side (see Figs. 1 and 2); instead, the left tributed to the gland, encircling it (from both the ascending artery was seen closely related to the ventral and the dorsal aspects) (Fig. 2). On its route esophagus. However, these differences did not make to the suprarenal gland, the suprarenogenital artery the features of the left IPA substantially different issued another branch, the superior genital branch, from the right IPA, and thus a further description which coursed along the ventral aspect of the upper seems to be superfluous, and will not be repeated . pole of the kidney (Fig. 2). After leaving the kidney, the superior genital branch bent slightly downwards to reach the diaphragmogenital ligament which was attached superiorly to the lateroinferior portion of 4 S. Mizukami et al .

Fig. 1. A diagrammatic representation of the IPA of female rats; a detailed configuration of this artery represents the meticulous findings obtained in this macroscopical study. The areas circled by dots just above the suprarenal glands are seen on both sides, indicating the supposed areas of the diaphragm where the closure of the pleuroperitoneal canals has taken place. The Inferior Phrenic Artery' of Female Rats 5

Fig. 2. A simplified representation of Figure 1. In this figure, only the representative branches of the ITA arc diaerammatically shown. The ITA is seen emitting 4 main arteries — i.e., the decending, suprarenal, suprarenogenital and descending arteries. Notc that the suprarenal as well as the suprarenogenital arteries issue superior and inferior genital branches, respectively, which descend in the diaphragmogonadal ligament to become contiguous with branches of the ovarian artery. The areas circled by dots indicate portions which have been formed by a closure of the dorsal and ventral pleuroperitoneal folds. 6 S. Mizukamiet al.

Discussion ships of this artery with the structures of the sur- rounding area which are deemed to be importantly The fundamental aim of this study was: involved in the development of IPA. In this con- 1. to clarify the general features of the inferior nection, Felix (1912) made an detailed, very important phrenic artery (IPA) of full-grown female rats which description on the development of the mesonephric seems to retain the original features established in arteries which were formed, in concomitant with the early stages of development; the development of the mesonephroi, from the 6th 1 to compare these features of the IPA of the thoracic to the 3rd lumbar segments. According to female rat with those of the human IPA in order to his findings, the human IPA is derived from the consider the IPA's potential to supply blood to the uppermost groups of these arteries, while from neighboring structure which are importantly involved the lower groups are formed the suprarenal, renal, in the development of this artery; and accessory renal, gonadal, accessory gonadal arteries, 3. to find reasons for the occurrence of aberrant and also the branches to the lymph nodes and the branches of the human IPA which are occasionally sympathetic ganglia in the region between the superior found to be destined for the urogenital organs. and inferior mesenteric arteries. In his detailed This macroscopical study elucidated the general work, however, he did not refer to topographic features of the IPA of female rats which, to our relationships of the developing IPA with the dia- knowledge, have not yet been described. Branches phragm and the inferior caval vein. Thus we dared of the IPA and their destinations found in this study conjecture a configuration of humans IPA in the were tabulates (see Table). This table clearly demon- early stage of development by combining the des- strates that the IPA of female rats supplies blood to cription reported by Well (1954), Gatonne (1984) more organs and structures than the name implies. and Felix (1912) with our observations of the IPA of Such a broad blood supply by the IPA seems to be female rats used in this study. Figure 3 illustrates the attributed to a multiplicity of topographical relation- topography of the developing suprarenal gland, the

Table Branching and distributions of the 4 major arteries arising from the inferior phrenic artery of female adult rats The Inferior Phrenic Artery of Female Rats 7

Fig. 3. A conjectured figure combining descriptions by Felix (1912), Wells (1954) and Gatonne (1984), and findings obtained in this study. In this Figure are shown the intimate relationships of the branches of the ITA to the ventral and dorsal pleuropericardial folds, the caval venous mesentery, the suprarenal glands, the gonad, and to the mesoncphros with mesonephric duct and ductuli. Close relationships to be emphasized are as follows: between the ascending artery and the caval venous mesenten as well as the ventral pleuroperitoneal fold; between the suprarenal artery and dorsal pleuroperitoneal fold; between the suprarenogenital artery and the genital tract; between the descending artery and the genital tract. 8 S. Mizukamiet al. gonad, the mesonephroi with ductuli and ducts, and importance should be attached to the close intimacy the transverse septum, and the dorsal and ventral of the IPA with the inferior caval vein also in the pleuroperitoneal folds, and the inferior caval mes- human anatomy. entery, and simultaneously the following main A further important feature of the ascending arteries of the IPA observed in this study: (1) as- artery of the IPA of female rats is its apparent cending artery; (2) suprarenal artery; (3) supra- relationship with the ventral pleuroperitoneal renogenital artery; and (4) descending artery. The fold. The caval mesentery is said to be connected following discussion will be made on the relationships superiorly to the primitive right lobe of the liver, between these arteries and the embryological struc- and inferiorly to the mesonephroi (Arey, 1966), tures depicted in Figure 3. leading via or in close proximity of the ventral pleuroperitoneal fold (Uskow, 1883; Bremer, 1943; Ascending artery Gatonne, 1984), which, together with the dorsal The ascending artery could be considered to be fellow fold of the same side, is said to play an im- the direct continuation of the IPA. This artery was portant role in closing the pleuroperitoneal canal, found to play a principal role of supplying blood and accomplishes the separation between the pleural to the diaphragm. The key feature of this artery and peritoneal cavities. This fact leads us to a sup- is that it coursed upwards in accompanying the position that the ascending artery of the IPA of phrenic nerve throughout its entire course on the female rats has been critically involved in the com- medial lumbar crus and partes sternalis et costalis of pletion of the closure of the pleuroperitoneal canal. the diaphragm. The partes sternalis et costalis of the diaphragm were reported to be formed from the Suprarenal artery connective tissue anlage (die bindegewebige Pri- The important feature of the suprarenal artery of mitivanlage, Uskow, 1883) of the transverse septum female rats is that this artery took its course laterally and the musculus diaphragmaticus (Uskow, 1883), along the superior margin of the suprarenal gland, the anlage of the latter being derived from the while giving off numerous superior suprarenal myotomes at the level of the 4th and 5th (Gottschall ramusculi to this gland, and that it reached to the and Gruber, 1977) or 4th to 6th cervical segments. lateroinferior portion of the pars costalis of the Thus, it could be speculated that the ascending artery diaphragm, ending here by dividing into fine branches. is involved in the formation of the diaphragm. How- This portion of the diaphragm is described as having ever, the exact manner of involvement of this as- originated from the connective tissue anlage of cending artery still remains to be elucidated by the transverse septum and in addition from the further embryological studies. myogenic anlage of the musculus diaphragmaticus Another important configuration of this artery is located at lower cervical level segments (Laskowski, its intimate association with the inferior caval vein 1987). In this connection, and of fundamental im- on the right side, being located in the caval venous portance, is that these anlages have been located mesentery, a finding which strongly suggests that inferior or more strictly lateroinferior to the dorsal the ascending artery of the female rat has been pleuroperitoneal fold which is known to develop importantly involved in formation of the upper immediately above the mesonephric ridge and, very segment of this vein. This fact leads us to the sup- importantly, immediately above the attachment of position that the topographical approximation of the diaphragmogenital ligament (Patten, 1946). This the IPA to the inferior caval vein and its measentery dorsal pleuroperitoneal fold is known to extend onto as is observed in full-grown female rats, could be the dorsal body wall of embryos and to unite with expected to occur also in the anatomy of human the ventral pleuroperitoneal fold, thus accomplishing adults. In this connection, it is interesting to note pleuroperitoneal canal closure. This closure is sim- that in the anatomy the IPA is described as emitting ultaneously enhanced by the enlarging suprarenal a few twigs to the inferior caval vein (Williams et al. gland (located inferior and dorsomedial to this canal) 1989). Moreover, it is said that the homologous (Gatonne, 1984). To our knowledge, there is no inferior caval mesentery develops in early stages of literature available which affords evidence for the human embryos, paving the way for a connective topographical intimacy between the pleuroperitoneal vein between the subcardinal vein and the hepatic fold and the developing human IPA. According to vein, thus forming the upper segment of the inferior Hollinshead (1962), however, it is strongly suggested caval vein in the inferior caval mesentery (Evans, that the lateroinferior portion of the pars costalis of 1912). In view of this, it is very likely that the devel- the human diaphragm is supplied by branches of the oping artery of the human IPA (corresponding to superior suprarenal artery. the ascending artery of female rats) takes its course On the basis of this supposition, it could be stated in the caval mesentery. In any event, greater that the suprarenal artery of the IPA, like the above The Inferior Phrenic Artery of Female Rats 9 mentioned ascending artery, has been importantly species of rodents as well as of humans could be involved in the closure of the pleuroperitoneal canal. explained in connection with the events involved in: (1) the development of the diaphragm and the closure Suprarenogenital artery of the pleuroperitoneal canal by the ventral and The principal finding of this study is that the IPA dorsal pleuroperitoneal folds; (2) the enlargement of female rats holds a potential for blood supply to of the suprarenal gland; (3) the descent of the gonad the genital tract by giving off a superior genital and the genital tract while the mesonephroi regressing; branch which, after crossing the ventral or dorsal and (4) the formation of the inferior caval vein in aspect of the upper pole of the kidney, reached the the caval venous mesentery. diaphragmogonadal ligament. Very, notably, this In conclusion, it should be mentioned that the superior genital branch took their course in this IPA of female rats affords a quite beneficial means ligament to become contiguous with branches of the for considering the morphology of the IPA of human ovarian artery. In leading textbooks of the human beings, and for findng a vantage point for explaining embryology (Hamilton Mossman, 1978; Patten, the causative background of the aberrant branches 1953; Hinrichsen, 1990), the diaphragmogenital of this artery from the developmental point of view. ligament is named simply the diaphragmatic liga- ment. This ligament is said to develop in the early stages of human embryos (Hamilton Mossman, References 1978; Patten, 1953; Wartenberg, 1990; Wells, 1954), 1) Arey, L. B.: Descentof the gonads.In: Developmental but to undergo regression in later stages of devel- Anatomy.,7th ed. (ed. L. B. Arey). 332-335. Saunders. opment, thus leaving in human adults only its in- Philadelphia,1966. feriormost part — the suspensory ligament (Hamilton 2) Bock,P.: Zuckerkandl'sorgan. In: The Paraganglia(ed. & Mossman, 1978). This regressed portion of the P. BOO. 131-132. Springer. Heidelberg, 1982. ligament, however, might still hold a potential of 3) Bremer, J. L.: Pleuro-peritonealmembrane and bursa affording the human IPA a descending pathway infracardiaca.Anat. Rec., 87: 311-319, 1943. 4) Evans, H. M.: Transformationof the posteriorcardinal destined for the genital tract. This opinion is sup- veins.In: Manualof HumanEmbryology (ed. F. Kcibel & ported by the reports on an aberrant testicular artery F. P. Mall).vol. 2. 681-685.Lippincott. Philadelphia. 1912. of a Japanese human adult (Shinohara et al. , 1990) 5) Felix,W.: Thedevelopment of the urinogenitalorgans. In: and on an aberrant artery which, arising from the Manualof HumanEmbryology (ed. F. Keibeland F. P. "suprarenal" artery coursed toward the ovary Mall).752-979. Lippincott Co., Philadelphiaand London. 1912. (Hanle et al., to be published), both taking courses 6) Gatonne, W. H., & D. Morse. Pleuroperitonealcanal to the genital tract or the gonad that are strikingly closurein the rat. Anat. Rec., 208: 445-460, 1984. similar to that taken by the suprarenogenital artery 7) GottschalJ., & Gruber,H.: Theaccessory phrcnic nerve in of female rats. the rat. Anat.Embryol., 151: 63-69, 1977. 8) Hamilton,W. J., & Mossman,H. W.: Intraembryonic coelom.In: HumanEmbryology. 4th ed. (ed. 0. Hamilton, Descending artery H. W. Mossman).364-372. Williams & Wilkins. Baltimore. An important feature of the descending artery, in 1978. addition to giving off the inferior genital branch to 9) Hattie,A. Y. andYamadori, Y. Uniquecase of the ovarian the diaphragmogenital ligament, is its coursing along artery with variationof the suprarenalarteries. (to he with the major splanchnic nerve to reach the celiac published). 10) Hinrichsen,K. V.: Artericn des Rumplesund der Glide- ganglion. However, to our knowledge, there is no massen.In: Humanembryologie(ed. K. V. Hinrichsen) . evidence which explains the close intimacy of this 293-304.Springer. Berlin, 1990. artery with these nerve structures. One possibility 11) Hollinshead,W. H.: Diaphragm.In: Textbook of Anatomy is that in its development the descending artery (ed. W. H. Flollinshead).706-710. Harper & Row. New might have been involved in the formation of the York, 1962. 12) Laskowski,M. B., & Sanes, J. R.: Topographicmapping paraganglia, which are known to develop conspi- of motorpools onto skeletalmuscles. J. Neuroscience 7: cuously in the embryonal period, by supplying 252-260,1987. blood to them (Bock, 1982). However, there is no 13) Moore,K. L. Descendof the ovary.In: The Developing embryological literature available which affords Human. 3rd ed. (ed. K. L. Moore). 292 . Saunder. evidence of a blood supply to these ganglia by the Philadelphia.1988. 14) Patten.B. M.: Body cavities. Internal reproductive organs . descending artery of the IPA; Thus further studies In: HumanEmbryology. (ed . B. M. Patten). 499-510. are required for obtaining direct evidence for this 575-599.Blakiston Co., Philadelphia.1946. supposition. 15) Shinohara,M., Nakatani, T., Fukuo,Y ., S. Morishita,& T. Matsuda:Case with a high-positionedorigin of the On the basis of the findings of the IPA of female testicularartery. Anat. Rec., 226: 2M— '(6 rats obtained in this discussion, it could be concluded , 1990. 16) Uskow,U.: Ucher die Entwickclung des Zwerchfells , des that the multiplicity of branches of the IPA of this Pericardiumsund des Coeloms. Archir f. mikroskop . 10 S. Mizukami el al.

Anat., 22: 143-227, with plates 3-8, 1883. GA gonadal artery 17) Wartenberg, H.: Entwicklung der Genitalorgane und iGB inferior genital branch Bildung der Gamenten. In Humanembryologie (ed. K. V. ICV (circled) inferior caval vein Hinrichsen). 745-822. Springer. Berlin, 1990. IPA inferior phrenic artery 18) Wells, L. J.: Development of the human diaphragm and isr inferior suprarenal ramuli pleural sacs. Contribution to Embryology 35, 107-144, ITA internal thoracic artery 1954. ML massa longitudinalis 19) Williams, P. L., Warwick, R., Dyson, M., & Bannister, L. MSN mesonephros H.: Coronary anastomoses. In: Gray's Anatomy. 37th MSND mesonephric duct ed. (ed. P. L. Williams, R. Warwick, M. Dyson & L. H. msr middle suprarenal ramuli Bannister), p. 731. Churchill Livingstone. Edinburgh, MTN metanephros London, 1989. 0 ovarium OA ovarian artery PER pleuroenteric recess (Williams et al.) PHN phrenic nerve Abbreviations PPA pericardiacophrenic artery A aorta PPCF pleuropericardial fold AA ascending artery R ren CB capsular branch RC rectum CT centrum tendineum sGB superior genital branch CVM caval venous mesentery SR suprarenal gland dPPLF dorsal pleuroperitoneal fold (Gatonne) SRA suprarenal artery DA descending artery ssr superior suprarenal ramuli DD dorsal diaphragm (Uskow) UT uterus DGL diaphragmogonadal ligament vPPLF ventral pleuroperitoneal fold (caval fold , Warwick) E esophagus VD ventral diaphragm (Uskow) G gonad