The name cranial ovarian suspensory ligaments in mammalian anatomy should be used only to indicate the structures derived from the foetal cranial mesonephric and gonadal ligaments.код для вставкиСкачать
THE ANATOMICAL RECORD 237:434-438 (1993) The Name Cranial Ovarian Suspensory Ligaments in Mammalian Anatomy Should Be Used Only to Indicate the Structures Derived From the Foetal Cranial Mesonephric and Gonadal Ligaments P. VAN DER SCHOOT Department of Endocrinology and Reproduction, Erasmus University Rotterdam, Faculty of Medicine and Health Sciences, P.O. Box 1738,3000 DR, Rotterdam, The Netherlands ABSTRACT The term ovarian suspensory ligament appears ambiguous when human adult anatomy textbooks are compared with human embryology or with general mammalian anatomy textbooks. The term ovarian suspensory ligament in laboratory rodents and domestic animals indicates homologous structures during foetal (the cranial mesonephric and gonadal ligaments) and later life (the cranial mesonephric ligament derivatives). In human foetal anatomy textbooks ovarian suspensory ligament is generally applied to this same ligament. However, in human adult anatomy textbooks ovarian suspensory ligament is widely applied to the part of the (uterine) broad ligament which contains the uterine and ovarian blood and lymphatic vessels and nerves. This inconsistency in human anatomy books raises confusion on the nature of the foetal and adult ovarian suspensory ligaments and inconsistencies in the description of the normal anatomical relationships of the ovaries between humans and other mammals. For the proper understanding of normal gonadal growth and development within the abdomen, it is important to maintain a consistent nomenclature of the cranial ovarian structures. The current practice in veterinary and other mammalian textbooks offers a solid point of departure. 0 1993 Wiley-Liss, Inc. Key words: Cranial suspensory ligament, Plica suspensoria ovarii, Diaphragmatic ligament, Human anatomy, Mammalian anatomy, Foetal anatomy THE DEVELOPMENT OF THE CRANIAL The suspensory ligament of the ovary in the current OVARIAN LIGAMENT human anatomy seems the authorized name (NN, 1989) of ". . . the part of the broad ligament of the Hertwig (1888), Bayer (1908), Robinson (1915), Tanuterus that extends from the tuba1 end of the ovary and dler (1923),and Hadziselimovic (1983)are among those the infundibulum of the uterine tube to the lateral wall unequivocally distinguishing the ligamentum suspenof the pelvis, transmitting the ovarian blood vessels, sorium ovarii from the remaining broad ligament. The nerves, and lymph vessels. The fold continues superi- latter structure is described to develop along the meorly over the external iliac vessels to become continu- dial side of the mesonephros and gonadal anlagen ous with the parietal peritoneum over the psoas muscle (Hertwig, 1888)and to contain, close to the hilum of the either in the subcecal fossa or behind the descending ovaries ". . . between its two layers the ovarian vessels colon. . . ." (Love11 Becker et al., 1986; see also Hewitt and nerves . . .', (Robinson, 1915). The detailed descripet al., 1965). Accordingly, human anatomy textbooks tion of the growth and development of the cranial ovafrom the last decades use this name to indicate the rian suspensory structures during foetal life provided easily recognizable vascular plica between the ovaries, by Weber (1898) leaves no doubt that the cranial mevia the brim of the pelvis minor, and the medial pos- sonephric ligament, together with the cranial ovarian terior abdomen wall at the level of the major vessels of ligament on top of the mesonephros, forms the anlage the kidneys (e.g., Lockhardt et al., 1959; Hamilton et from which the cranial suspensory ligament develops. al., 1966; Thiel, 1969; Basmajian, 1971; Romanes, This cranial suspensory ligament is, structurally and 1981; Rohen and Yokochi, 1988; Fig. 1).This definition developmentally, different from the remaining broad of the ovarian suspensory ligament is surprising if this ligament (including the mesovarium, mesosalpinx and nomenclature is considered (1)in a developmental perspective, and in relationship to (2)data available in the general mammalian literature, and (3)the description of human and other mammalian foetal gonadal and Received December 7, 1992; accepted J u n e 8, 1993. genital development. 0 1993 WILEY-LISS, INC CRANIAL OVARIAN SUSPENSORY STRUCTURES Fig. 1. View of the lateral side of the female abdomen. The suspensory ligament ofouary is shown to contain the ovarian vasculature and nerves. This paper argues that more properly only the cranial side of this structure deserves this name, while the remaining structure should be considered part of the broad ligament. The proper cranial or mesuterinum) which carries the ovarian, tuba1 and uterine vasculature and innervation and which develops from the coelomic epithelium covering the mesonephros and developing gonad on their medial aspect. Throughout the human anatomical literature different names have been attributed to the part of the broad ligament with the ovarian vessels: plica suspensoria ovarii (Sieglbauer, 1935; Pernkopf, 1941 and 1980, [but not in its last edition (Pernkopf, 1989)l; Hochstetter, 1940), plica vascularis (Hadziselimovic, 1983), infundibulo-pelvic fold (Last, 1984), or ligament (Ellis, 1992). 435 suspensory ligament can be seen, as described earlier, to “. . . get lost in the peritoneum covering the external iliac vessels and the psoas muscle. . . .” (Robinson, 1915). (Reproduced, by permission of Oxford University Press, from Romanes, 1981, page 565, Fig. 8.52.) cow and pig: Getty, 1975; cat: Crouch and Lackey, 1969; hedgehog: Weber, 1904; guinea pig: Cooper and Schiller, 1975; rat: Hebel and Stromberg, 1976; hamster: Hoffman et al., 1968; mouse: Brambell, 1927; Cook, 1965). It has the function to suspend the ovary while the remaining broad ligament only serves to unite the different component parts of the gonads and Wolffian or Miillerian duct derivatives (Evans and Christensen, 1979). The suspensory ligament contains smooth muscle cells and elastic fibres (Hebel and Stromberg, 1976), and is well developed in animals with ovaries close to the caudal pole of the kidney (such as horse, dog, and cat, and laboratory rodents), whereas THE MAMMALIAN OVARIAN SUSPENSORY LIGAMENT poor development is noticed in animals with ovaries In veterinary and other mammalian anatomy text- more caudal in the abdomen (pigs, cows, primates). In books the term suspensory ligament of the ovary is gen- males without testis descent (so-called testiconda-like erally applied to “. . . the cranial portion of the free elephants and whales) cranial testis suspensory ligaborder of the broad ligament” (Ellenberger and Baum, ments (Umierenbunde) are well developed (Weber, 1915; Getty, 1975; Evans and Christensen, 1979). In a 1904). In all these female mammals the anastomosing variety of species this ligament connects the upper por- ovarian and uterine vasculature and nerves cross the tion of the ovary, via a route lateral to the kidney, to broad ligament just as in human females into craniothe ipsilateral part of the diaphragm at the junction of medial direction, but no specific name is attributed to the middle and last third of the last rib (dog: Evans and this (vascular, nervous, and lymphatic vessel) complex. Christensen, 1979; horse: Ellenberger and Baum, 1915; Evidently the term suspensory ligament of the ovary is used to indicate different structures when human anatomy or the anatomy of other mammals is considered. It can be added that according to some (van den Broek, 1933; Starck, 1982) but not to others (Weber, 1904), reptiles, without testicular descent, have their kidneys caudal to the level of the gonads, and show obvious cranial testicular suspensory ligaments. THE SUSPENSORY LIGAMENT DURING MAMMALIAN FOETAL LIFE During mammalian foetal life the gonads develop in close association with the ventromedial surface of the mesonephroi. These latter organs develop as prominences, to both sides of the midline, on the posterior body wall with easily identifiable ligaments a t their caudal and cranial sides. The major vascular and nervous connections develop along their medial sides (e.g., Patten, 1948). The gonads develop caudal and cranial ligaments merging with the surface epithelium of the mesonephros (Weber, 1898). During mesonephric regression these gonadal ligaments fuse with the remnants of the earlier mesonephric ligaments (Weber, 1898; van den Broek, 1933; Patten, 1948). After mesonephric regression cranial gonadal ligaments, together with remnants of the earlier mesonephric ligaments, are unequivocally distinguishable in both human and other mammalian foetuses between the cranial pole of the gonads and the crura of the developing diaphragm. Several names have been used in females to indicate these structures such as: the ovario-pelvic ligaments (Gegenbaur, 1899),the lumbo-ovarian ligaments (Rouviere, 19241, the cranial mesonephric ligaments (Blechschmidt, 1961), the cranial gonadal suspensory ligaments (e.g., Hamilton et al., 19661,the cephalic gonadal ligaments (Gier and Marion, 1970), and the diaphragmatic ligaments (Patten, 1948; Netter 19651, or the plicae diaphragmaticae (Weber, 1904; Brambell, 1927) or Zwerchfellbande in German literature (Hertwig, 1888;Weber, 1898; Tonutti et al., 1960). The last three names specifically reflect the connection, existing through these ligaments, between the developing gonads and the diaphragm (Cooper and Schiller, 1975; Hebel and Stromberg, 1976). The ligaments run lateral to the kidneys and do not contain the major ovarian vessels or nerves which pass between the gonads and the medial aspect of the developing kidneys (pig: Patten, 1948; human: England, 1983 and Hinrichsen, 1991). They are present similarly in early female and male foetuses (Weber, 1904; Patten, 1948; Blechschmidt, 1961; Netter, 1965; England, 1983; Renfree and Short, 1988). They disappear completely in males with descended testes but remain unequivocally distinguishable in developing and adult females of all species mentioned in the previous paragraph including minor remnants in humans (Robinson, 1915; Romanes, 1981; Hadziselimovic, 1983; Hinrichsen, 1991; Fig. 1). DISCUSSION The nomenclature of the cranial gonadal ligaments in fetal and adult sub-human mammalian species is consistent as the term cranial ovarian suspensory ligament refers to the structure developing from the cranial mesonephric ligament. The term suspensory ligament is functionally appropriate: it can be easily demonstrated that the ligament plays a role to keep the ovary at a position in the abdomen a t some distance from the posterior and the lateral body wall (dog: Evans and Christensen, 1979; cow, pig, and horse: Getty, 1975) as well as at a fair distance from the caudal midline as required by the bicornuate elongated uterus. In contrast, in humans the nomenclature before and after birth is confusing: in fetal anatomy the “cranial ovarian suspensory ligament” refers to the earlier cranial mesonephric ligament and in adult anatomy to the structure developing from the medial part of the mesonephric peritoneal fold containing the vessels and nerves. The discussion about this inconsistency is not new (see, e.g., Tandler, 1923) but has apparently been insufficient to lead to a consensus. The inconsistency between the human foetal and adult nomenclature may underlie the apparent ambiguities in the interpretation of the nature of the developing and adult gonadal ligaments present at the lateral and the medial side of the kidney. In one of the widely used standard texts on human embryology it is supposed that the embryonic suspensory ligaments atrophy and become replaced by the adult suspensory ligaments containing the ovarian vasculature (Hamilton et al., 1966). Other texts contain the unjustified suggestion, that the adult suspensory ligament develops from the embryonic suspensory ligament (Braus, 1924; Sadler, 1990) or even from the female gubernaculum (Attah and Hutson, 1991) while these structures have a different embryological origin as argued above (Weber, 1898; Tandler, 1923; Harrison, 1963; Hadziselimovic, 1983). Schematic drawings of ovarian ligament development in humans are sometimes incorrect because of the unjustified interpretation of the identical nature of the foetal and postnatal suspensory ligament (Hinrichsen, 1991). Other mammalian textbooks would never, and do not indeed, present such pictures and statements as no doubt can rise on the different nature of the foetal cranial gonadal suspensory ligaments and the gonadal vascular plica (e.g., Ellenberger and Baum, 1915; Crouch and Lackey, 1969; Cooper and Schiller, 1975; Evans and Christensen, 1979; Evans and Christensen, 1979). There might be a specific reason why the foetal cranial ovarian suspensory ligaments become inconspicuous in humans (and in other primates as well, see e.g. Hartman and Straus, 1933; Hill, 1953) as compared with many other mammals. Humans (and primates in general) are exceptional in their possession of a uterus simplex with the ovaries situated a t an unusually far caudal position in the abdomen a t the entrance of the pelvis minor (compare, e.g., human situation in England [19831or rhesus monkey in Hartman and Straus with that of cats in Crouch and Lackey  or guinea pigs in Cooper and Schiller ). Together with the upright body posture, ovarian support will come predominantly from the close attachment of the organs to the immediately surrounding abdominal wall and pelvic bony structures. Laterally, the curvilinear course of the string of ovarian vasculature, nerves and lymphatic vessels (see Love11 Becker et al., 1986) keeps the ovaries closely adhering to the lateral body wall. Medially, ovaries are fixed to the uterus through the Ligamentum ovarium proprium and, further, to the ventral body wall through the Ligamentum teres uteri. CRANIAL OVARIAN SUSPENSORY STRUCTURES Caudally and posteriorly, the ovaries get support from the adjacent bony pelvic structures. Consequently, there is no need for further ovarian suspension to the cranio-lateral abdomen and this is the kind of support provided specifically by the cranial ligaments in all other mammals mentioned before. The ample further ovarian support makes it easy to understand that the foetal cranial ovarian suspensory ligaments “. . . get lost in the peritoneum covering the external iliac vessels and the psoas muscle. . . .” (Robinson, 1915) during further development to become such inconspicuous structures (see pictures, for example, in Netter, 1965; Dox et al., 1979; Romanes, 1981; Rohen and Yokochi, 1988) as to become not recognized any more a s relevant structures between the ovaries and the cranio-lateral part of the abdomen (Basmajijan, 1971). The proper distinction, however, between the cranial suspensory ligament and the remaining broad ligament could appear of a significance in the near future: recently evidence has been obtained, in rats, of the specific sensitivity of the foetal cranial suspensory ligament to androgen (van der Schoot and Elger, 1992). It appeared t h a t prenatal androgens were responsible for their failure to grow in male animals. Further work should reveal whether androgen sensitivity of the developing cranial gonadal suspensory ligament is of interspecific generality. RECOMMENDATION For the proper understanding of the development of the cranial gonadal ligaments from foetal to adult life it is preferable to distinguish unequivocally between the cranial ovarian suspensory ligament derived from the cranial mesonephric and foetal gonadal ligament and the further broad ligament containing, among others, the plica carrying the ovarian vasculature and nerves and developing from the medial part of the mesonephric peritoneal fold. Such distinction is unavailable in much of the current human anatomy textbooks but obviously present in the other mammalian literature. Another term, if any beyond ovarian vessels (Romanes, 1981) would be required, should be reserved to indicate the conspicuous primate-specific fold which contains the ovarian vasculature, nerves, and lymphatic vessels and which offers, through the unusually low position of the ovaries in the primate body cavity, a ligament-like connection between the ovaries and the posterior abdomen midline. In accordance with the nomenclature of the earlier editions of Pernkopf Anatomie (1941, 1980) and Hochstetter (1940) the latter structure could be indicated as the plica suspensoria ovarii. Another possibility could be to apply the name plica vasculosa ovarii or plica vascularis ovarii to it: in the veterinary nomenclature (NN, 1983) this name indicates the plica containing the testicular vessels in males and its use in females would stress the homology between the sexes with respect to this vascular structure. If plica suspensoria ovarii would be accepted a further problem should be solved with respect to the human Nomina anatomica embryologica (NN, 1989).The term plica suspensoria ovarii appears in this list to indicate the structure proposed above to being called the foetal cranial ovarian suspensory ligament. Fortunately, however, this problem could be overcome with- 437 out too much difficulty: as far as the present author has learned from scrutinizing current textbooks in human embryology, this apparently authorized name for the cranial mesonephric ligament derivatives has not gained recognition, and books generally refer to this structure as the ovarian suspensory or diaphragmatic ligament (e.g., Netter, 1965; Hamilton et al., 1966; Corliss, 1976; England, 1983; Sadler, 1990; Hinrichsen, 1991) except when naming this suspensory structure has apparently not been considered (e.g., in Wendell Smith and Williams, 1984; Beck et al., 1985). ACKNOWLEDGMENTS Dr. M. Schalekamp and Dr. R. Stoeckart (Anatomy Department of the Erasmus University) and Prof. Dr. M.J. de Jongh (Embryology Department, State University of Groningen) are cordially thanked for stimulating discussions during the preparation of this manuscript. LITERATURE CITED NN 1983 Nomina anatomica veterinaria, 3rd ed., International Committee on Veterinary Gross Anatomical Nomenclature. Ithaca, New York. NN 1989 Nomina Anatomica. 5th ed., International Anatomical Nomenclature Committee. Churchill Livingstone, Edinburgh. Attah, A.A., and J.M. Hutson 1991 The anatomy of the female gubernaculum is different from the male. Australian N Zealand J Surg, 61t380-384. Basmajian, J.V. 1971 Grant’s Method of Anatomy, 8th ed., Williams and Wilkins, Baltimore. Bayer, H. 1908 Entwicklungsgeschichte und Anatomie des weiblichen Genitalapparates. Schlesier, Strassburg. Beck, F., D.B. Moffat, and D.P. Davies 1984 Human Embryology, 2nd ed. Blackwell, Oxford. Blechschmidt, E. 1961 The Stages of Human Development Before Birth. Karger, London. Brambell, F.W.R. 1927 The development and morphology of the gonads of the mouse. 2: The development of the Wolffian body and ducts. Proc. Roy. SOC. Lond. B., 102t206-221. Braus, H. 1924 Anatomie Des Menschen. Springer, Berlin. Broek, A.J.P. van den 1933 Urogenitalsystem Vol. 6, Ch 1 p. 1-154. In: Handbuch der Vergleichenden Anatomie der Wirbeltiere. L. Bolk, E. Goppert, E. Kallius, and W. Lubosch, eds. Urban & Schwarzenberg, Berlin. Cook, M.J. 1965 The Anatomy of the Laboratory Mouse. Academic Press, London. Cooper, G., and A.L. Schiller 1975 Anatomy of the Guinea Pig. Harvard University Press, Cambridge, Massachusettes. Corliss, C.E. 1976 Patten’s Human Embryology. McGraw-Hill, New York. Crouch, J.E., and M.B. Lackey 1969 Text-atlas of Cat Anatomy. Lea and Febiger, Philadelphia. Dox, J., B.J. Melloni, and G.M. Eisner 1979 Melloni’s Illustrated Medical Dictionary. Williams and Wilkins, Baltimore. Ellenberger, W., and H. Baum 1915 Vergleichende Anatomie der Haustiere. Hirschwald, Berlin. Ellis, H. 1992 Clinical Anatomy, 8th ed. Blackwell, London. England, M.A. 1983 A Colour Atlas of Life Before Birth. Wolfe, London. Evans, H.E., and G.C. Christensen 1979 Miller’s Anatomy of the Dog, 2nd ed. Saunders, Philadelphia. Gegenbauer, C. 1899 Lehrbuch der Anatomie des Menschen. Engelmann, Leipzig. Getty, R. 1975 The Anatomy of Domestic Animals, 5th ed. Saunders, Philadelphia. Gier, H.T., and G.B. Marion 1970 Development of the mammalian testis. In: A.D. Johnson, W.R. Gomes, and N.L. VandeMark, eds. The Testis, Vol 1. Academic Press, New York, pp. 1-45. Hadziselimovic, F. 1983 Embryology of testicular descent and maldescent. In: Cryptorchidism, management and implication. F. Hadziselimovic, ed. Springer, Berlin, pp. 11-34. Hamilton, W.J., J.D. Boyd, and H.W. Mossman 1966 Human Embryology. Heffer, Cambridge UK. Harrison, R.G. 1963 A Textbook of Human Embryology. Blackwell, Oxford. Hartman, C.G., and W.L. Straus 1933 The Anatomy of the Rhesus Monkey. Hafner, New York. Hebel, R., and M.W. Stromberg 1976 Anatomy of the Laboratory Rat. Williams and Wilkins, Baltimore. Hertwig, 0. 1888 Lehrbuch der Entwicklungsgeschichte des Menschen und der Wirbeltiere. 3rd ed. Fischer, Jena. Hewitt, R.H., E.C.L., Miller, and A.H. Sanford 1965 Dorland’s Illustrated Medical Dictionary. S a n d e r s , Philadelphia. Hill, W.C. 1953 Primates, Comparative Anatomy and Taxonomy. Edinburgh, University Press. Hinrichsen, K.V. 1991 Humanembryologie. Springer, Berlin. Hochstetter, F. 1940 Toldt’s Anatomischer Atlas, 18th ed. Urban and Schwarzenberg, Berlin. Hoffman, R.A., P.F. Robinson, and H. Magalhaes 1968 The Golden Hamster. Its biology and Use in Medical Research. Iowa State University Press, Ames, Iowa. Last, R.J. 1984 Anatomy, 7th ed. Churchill Livingstone, Edinburgh. Lockhardt, R.D., G.F. Hamilton, and F.W. Fyfe 1959 Anatomy of the Human Body. Faber and Faber, London. Love11 Becker, E., W.J.H. Butterfield, A. McGehee, R.H. Heptinstall, and L. Thomas 1986 International Dictionary of Medicine and Biology. J . Wiley and Sons, New York. Netter, F.H. 1965 Ciba Collection of Medical Illustrations, Vol. 2: Reproductive system. Summit, New Jersey. Patten, B.M. 1948 Embryology of the Pig. McGraw-Hill, New York. Pernkopf, E. 1941 Topographische Anatomie des Menschen. Urban and Schwarzenberg, Berlin. Pernkopf, E. 1980 Topographische Anatomie des Menschen, 2nd ed. H. Ferner ed., Urban and Schwarzenberg, Berlin. Pernkopf, E. 1989 Atlas of topographical and applied human anat- omy, 3rd ed. W. Platzer ed., Urban and Schwarzenberg, Baltimore. Renfree, M.B., and R.V. Short 1988 Sex determination in marsupials: evidence for a marsupial-eutherian dichotomy. Phil. Trans. R. SOC. Land., B 322t41-53. Robinson, A. 1915 Cunningham’s Textbook of Anatomy, 4th ed. Frowde, Hodder and Stoughton, Edinburgh. Rohen, J.W., and C. Yokochi 1988 Human Anatomy. Schattauer, Stuttgart. Romanes, G.J. 1981 Cunningham’s Textbook of Anatomy, 12th ed. Oxford University Press, Oxford, United Kingdom. Rouviere, H. 1924 Anatomie Humaine Descriptive et Topographique. Masson, Paris. Sadler, T.W. 1990 Langman’s Medical Embryology, 6th ed. Williams and Wilkins, Baltimore. Sieglbauer, F. 1935 Lehrbuch der Normalen Anatomie des Menschen. Urban and Schwarzenberg, Berlin. Starck, D. 1982 Vergleichende Anatomie der Wirbeltiere. Springer, Berlin. Tandler, J. 1923 Lehrbuch der Systematischen Anatomie. Vogel, Leipzig. Thiel, W. 1969 Lehrbuch der topographischen Anatomie, 3rd ed. Springer, Berlin. Tonutti, E., 0. Weller, E. Schuchadt, and E. Heinke 1960 Die Mannliche Keimdruse. Thieme, Stuttgart. van der Schoot, P., and W. Elger 1992 Androgen-induced prevention of the outgrowth of the cranial gonadal suspensory ligaments in rats. J Andrology 13534-542. Weber, M. 1898 Studien uber Saugetiere. Fischer, Jena. Weber, M. 1904 Die Saugetiere. Fischer, Jena. Wendell Smit, C.P., and P.L. Williams 1984 Basic Human Embryology, 3rd ed. Pitman, London.