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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.

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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
[1933]with that of cats in Crouch and Lackey [1969] or
guinea pigs in Cooper and Schiller [1975]). 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.
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