The oviduct (uterine tube) revisited
Keywords: equine, mare, oviduct, uterine tube
The Nomina Anatomica Veterinaria refers to this structure as the uterine tube (to distinguish it from the oviduct of birds). However, that term is seldom used in either practice or publication. In both humans and animals, it is instead referred to as the oviduct. The oviduct in any species is amazing but even more so in mares. This entry substantiates that impression.
As shown in figure 1, the oviduct runs within the ovarian bursa, almost parallel to its margin but a full centimeter or more away.
Figure 1 is labeled above. Divisions of the oviduct (infundibulum, ampulla etc) shown here are those adopted from, and and described in: Aguilar, J.J. et al. 2012. Histological characteristics of the equine oviductal mucosa at different reproductive stages. J.Equine.Vet. Sci. 32:99-105. Note: The ovary in situ hangs from the mesovarian ligament so that the ovulation fossa faces ventrally. In this image, the ovary and bursa have been rotated as shown by the arrow in the small inset. The ovulation fossa is not yet visible despite this rotation. Image size: 1600 x 1041 px
The ovarian bursa can be likened to a lateral, low-drooping eyelid over an eye (the ovary). The long dimension of the ovoid-shaped ovary lies on a cranial-caudal axis. The cranial pole of this axis is slightly higher than the caudal pole. The infundibulum lies at the cranial pole of the ovary. As shown in figure 1, it is not attached to the ovary. In fact, it lies a remarkable distance from the ovulation fossa.
Figure 2: An oocyte, 150µ in diameter is shown at the end of the yellow arrow. This simulates the appearance of a real oocyte shortly after ovulation. Note its size relative to the infundibulum and ostium. Also note the cloud-like mass around the oocyte. This is a simulation of the large cumulus oophorus that accompanies the oocyte into the infundibulum. The cumulus is lost within 6 to 12 hours after the oocyte enters the oviduct (personal communication; Dr Katrin Hinricks). Image size: 1630 x 1236 px
When stretched out, the oviduct in a mare is a little longer than the human hand i.e. about 20 to 30 centimeters. It is a continuum with no distinct delineation. To facilitate functional descriptions however, it is divided into three main sections i.e. the infundibulum (L.< funnel), ampulla (L.< flask) and finally the isthmus (L.<neck of land between two seas) narrowing as it enters the uterus at a papilla that forms the uterotubal junction.
Figure 3: This figure includes a large section of the infundibulum and a smaller inset image of the isthmus. They are both at the same scale of magnification. Again, the author has modeled an oocyte in the infundibulum and in addition, an embryo in the isthmus. Both are visible beside black bars 150µ ling at the end of the yellow arrows. This was done to compare the size those structures with the histology of parts of the oviduct. The diameter of an equine oocyte is approximately 150µ; slightly larger than that a bovine oocyte (120µ). By day 6, the equine embryo is approximately 200µ in diameter. The white scale within each image is 500µ and the small bar adjacent to the oocyte and embryo is 150µ long. Image size: 4242 x 3090 px
The oviduct is of course, a conduit to transport oocytes, then embryos from the ovary to the uterus. But it is also an organ that performs the seemingly impossible task of (often simultaneously) transporting oocytes towards the uterus while promoting the ascent of spermatozoa from the uterus into the oviduct. Like other tubular organs throughout the body it has inner circular and outer longitudinal layers of smooth muscle that promote peristaltic movement. It also has within its mucosal lining, ciliated cells that also play a role in gamete transport. Presumably, peristaltic movements play a major role in transporting oocytes towards the uterus while cilia perform a major role with regard to the ascent of spermatozoa. However, the exact integration of these two propelling mechanisms has yet to be described.
It is known that spermatozoa ascend into the oviduct and bind to its epithelium, usually laying in wait for the oocyte to arrive after ovulation. It is possible for fertilization to occur when spermatozoa arrive in the oviduct up to 18 hours after ovulation (with post ovulation insemination) but it is far more common for spermatozoa to spend a day or two or even up to 7 days in the oviduct before ovulation. During that time, Ca++ fluxes within the oviduct suppress capacitation while gaseous exchange and nutrition keep spermatozoa viable. True, it is more likely that an oocyte will be fertilized with close synchrony between insemination and ovulation but the ability of the oviduct to keep spermatozoa viable for long periods of time is still remarkable; far superior than any device contrived by humans.
Capacitation and the release of spermatozoa from their binding sites on the oviduct epithelium is orchestrated by changes in the steroid milieu, especially increased progesterone production shortly before ovulation. The effect of the oviduct environment on spermatozoa is of critical importance in mares. Specifically (and peculiar to mares again) it is only in the oviduct that fertilization can occur. Therefore, unless spermatozoa are injected directly into oocytes (ICSI), in-vitro fertilization in horses is seldom successful.
Figure 2: A 16 gauge blunted needle is introduced into the ostium of the oviduct from a two-year-old mare. Blue dye is then introduced to outline the convoluted shape of the oviduct. Evidence of the dye in the uterus is shown as it permeates through to the serosa at the site marked B. This image defines the oviduct clearly. However the anatomical divisions (especially the ampullary-ithmic junction) so glibly discussed in literature, are far from obvious. Image size: 3456 x 2557 px
The uterotubal junction too, is a remarkable structure in mares. Spermatozoa deposited in the uterus are swept up to the uterotubal junction and are found in the oviduct within a few minutes of insemination. Yet, it is virtually impossible in normal mares, to force either fluid or air from the uterine lumen into the oviduct. This is because the oviduct of the mare is unique amoung domestic species with respect to its uterotubal junction. In mares, the distal oviduct has a well developed muscularis which acts as a sphincter, making mechanical entry from the uterus difficult. One can introduce fine tubes into the oviduct from the uterus but otherwise the uterotubal junction in mares acts as a one-way valve preventing fluid ascent from the uterus. To some degree, this may explain the relative lack of oviduct pathology in mares compared to cattle.
Alter about six and a half days in the oviduct, incubating mainly at the ampullary-ithmic junction, embryos enter the uterus. In mares of course, single embryos are far more common than twin embryos. At that time, late morulas or early blastocysts can be collected by flushing the uterus. Before that time it is impossible to retrieve a fertilized embryo by flushing the uterus alone.
Although unfertilized oocytes are occasionally found in the uterus, this is unusual. In general, if an oocyte is not fertilized in mares, it will not reach uterus. This phenomenon is unique among equids. Therefore it is generally not important to determine if oocytes have been fertilized when they are collected for embryo transfer. It is now universally recognized that production of prostaglandin E2 by embryos (not oocytes) causes relaxation of oviduct smooth muscle. This allows transport of the embryo into the uterus. When mares are examined postmortem, it is not unusual to find flattened, degenerate oocytes from previous cycles, caught within the oviduct.
Selected references:
Allen, W.E. et al. 1979. Evaluation of uterine tube function in pony mares. Vet. Record 105: 364-366
Arnold, C.E. and Love, C.C. 2013. Laparoscopic evaluation of oviductal patency in the standing mare. Theriogenology 79: 905-910
Bennett, S. 2002. Surgical evaluation of oviduct disease and patency in the mare. Proc. AAEP 48:347-349
Betteridge, K.J. 2000. Comparative aspects of equine embryonic development. Anim. Reprod. Sci. 60: 691-702
Brinsko, S,P. 1991. The effect of uterine lavage performed four hours post insemination on pregnancy rate in mares. Theriogenology 35: 1111-1119
Dobrinski, I. et al. 1997. Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biol. Reprod. 56: 861-869
Freeman, D.A. 1991. Time of embryo transport through the mare oviduct. Theriogenology 36: 823-830
Ghazal, S et al. Glob. libr. women's med., (ISSN: 1756-2228) 2014; DOI 10.3843/GLOWM.10317
Hinrichs, K. 2010. In vitro production of equine embryos: State of the art. Reprod. Domestic Anim 45: 3-8
Hunter, R.H.F. 1999 Ovarian follicular fluid, progesterone and Ca2+ ion influences on sperm release from the Fallopian tube reservoir. Gamete biology. 54: 283-291
Hunter, R.H.F. 2008. Sperm release from oviduct epithelial binding is controlled hormonally by peri‐ovulatory graafian follicles. Molecular Reprod. Devel. Incorporating Gamete Research 75: 167-174
Inoue, Y. 2013 Hysteroscopic hydrotubation of the equine oviduct. Equine Vet J. 45:761-765
Kenney, R.M. 1993. A review of the pathology of the equine oviduct. R. M. Kenney. Equine Vet. J. 25 (S15): 42-46
Leemans, B.M. 2015. Why doesn’t conventional IVF work in the horse? The equine oviduct as a microenvironment for capacitation/fertilization. Reproduction 152: R233-R245
Navara, K. J. 2015. Higher rates of internal ovulations occur in broiler breeder hens treated with testosterone. Poult Sci. 94:1346-1352
Rigby, S. et al. 2000. Oviductal sperm numbers following proximal uterine horn or uterine body insemination. Proc. AAEP. 46:332-334
Saltiel, A. et al. 1986. Pathologic findings in the oviducts of mares. Am. J. Vet Res. 47: 594-597
Sieme, H. et al. 2003. The effects of different insemination regimes on fertility in mares. Theriogenology 60: 1153-1164
Smits, K et al. 2016 The equine embryo influences immune-related gene expression in the oviduct. Biol. Reprod. 36: 1-8
Tsutsumi, Y. 1979. Evidence of the origin of the gelatinous masses in the oviducts of mares.
J. Reprod. Fert. 57: 287-290
Weber, J.A. 1995. Relaxatory effect of prostaglandin E2 on circular smooth muscle isolated from the equine oviductal isthmus. Biol. Reprod. Monograph. series1: 125-130
As shown in figure 1, the oviduct runs within the ovarian bursa, almost parallel to its margin but a full centimeter or more away.
Figure 1. The left ovary of a two year old mare, suspended under water. The ovulation fossa is invisible, pointing ventrally in the image. 2903 x 2054 px
Figure 1 is labeled above. Divisions of the oviduct (infundibulum, ampulla etc) shown here are those adopted from, and and described in: Aguilar, J.J. et al. 2012. Histological characteristics of the equine oviductal mucosa at different reproductive stages. J.Equine.Vet. Sci. 32:99-105. Note: The ovary in situ hangs from the mesovarian ligament so that the ovulation fossa faces ventrally. In this image, the ovary and bursa have been rotated as shown by the arrow in the small inset. The ovulation fossa is not yet visible despite this rotation. Image size: 1600 x 1041 px
| This anatomy never ceases to amaze the author. In essence, the infundibulum acts like a catcher's mitt in a baseball game, covering an ambitious area some distance from the pitcher's mound i.e. the ovulation fossa in this analogy. The baseball is of course, the oocyte. The infundibulum is well supplied with smooth muscle and engorged blood vessels during estrus, expanding the catcher's mitt. Yet the precise mechanism and magic behind the dependability of the catcher remains unknown and unseen. For those not familiar with baseball i.e. (insert nationality here), the author suggests consulting the book "Complete idiots guide to baseball and oocytes". It has been suggested that the fimbriae of the infundibulum sweep the surface of the ovary at the time of ovulation, picking up the oocyte in the process, moving it into the complex folds of the infundibulum. Although the frequency of loss of oocytes into the peritoneal cavity is unknown in mares, it probably does occur; it has certainly been documented in humans. Certainly, losses of oocytes into the peritoneal cavity is described in poultry, especially broiler hens. Interestingly, laying hens, selected for egg production are less prone to peritoneal loss of oocytes. In rodents and canids, oocyte-catching expertise by the infundibulim is less important than other species. This is because ovarian bursae in those animals surround their ovaries completely and are continuous with the infundibula themselves. This makes it impossible for their oocytes to escape into the peritoneal cavity. |
When stretched out, the oviduct in a mare is a little longer than the human hand i.e. about 20 to 30 centimeters. It is a continuum with no distinct delineation. To facilitate functional descriptions however, it is divided into three main sections i.e. the infundibulum (L.< funnel), ampulla (L.< flask) and finally the isthmus (L.<neck of land between two seas) narrowing as it enters the uterus at a papilla that forms the uterotubal junction.
The oviduct is of course, a conduit to transport oocytes, then embryos from the ovary to the uterus. But it is also an organ that performs the seemingly impossible task of (often simultaneously) transporting oocytes towards the uterus while promoting the ascent of spermatozoa from the uterus into the oviduct. Like other tubular organs throughout the body it has inner circular and outer longitudinal layers of smooth muscle that promote peristaltic movement. It also has within its mucosal lining, ciliated cells that also play a role in gamete transport. Presumably, peristaltic movements play a major role in transporting oocytes towards the uterus while cilia perform a major role with regard to the ascent of spermatozoa. However, the exact integration of these two propelling mechanisms has yet to be described.
It is known that spermatozoa ascend into the oviduct and bind to its epithelium, usually laying in wait for the oocyte to arrive after ovulation. It is possible for fertilization to occur when spermatozoa arrive in the oviduct up to 18 hours after ovulation (with post ovulation insemination) but it is far more common for spermatozoa to spend a day or two or even up to 7 days in the oviduct before ovulation. During that time, Ca++ fluxes within the oviduct suppress capacitation while gaseous exchange and nutrition keep spermatozoa viable. True, it is more likely that an oocyte will be fertilized with close synchrony between insemination and ovulation but the ability of the oviduct to keep spermatozoa viable for long periods of time is still remarkable; far superior than any device contrived by humans.
| As amazing as sperm preservation maybe in mares, it is overshadowed by the achievement of oviducts in other species. In some fruit bats in hibernation for example, spermatozoa can survive for weeks even months within the oviduct! |
Capacitation and the release of spermatozoa from their binding sites on the oviduct epithelium is orchestrated by changes in the steroid milieu, especially increased progesterone production shortly before ovulation. The effect of the oviduct environment on spermatozoa is of critical importance in mares. Specifically (and peculiar to mares again) it is only in the oviduct that fertilization can occur. Therefore, unless spermatozoa are injected directly into oocytes (ICSI), in-vitro fertilization in horses is seldom successful.
Figure 2: A 16 gauge blunted needle is introduced into the ostium of the oviduct from a two-year-old mare. Blue dye is then introduced to outline the convoluted shape of the oviduct. Evidence of the dye in the uterus is shown as it permeates through to the serosa at the site marked B. This image defines the oviduct clearly. However the anatomical divisions (especially the ampullary-ithmic junction) so glibly discussed in literature, are far from obvious. Image size: 3456 x 2557 px
The uterotubal junction too, is a remarkable structure in mares. Spermatozoa deposited in the uterus are swept up to the uterotubal junction and are found in the oviduct within a few minutes of insemination. Yet, it is virtually impossible in normal mares, to force either fluid or air from the uterine lumen into the oviduct. This is because the oviduct of the mare is unique amoung domestic species with respect to its uterotubal junction. In mares, the distal oviduct has a well developed muscularis which acts as a sphincter, making mechanical entry from the uterus difficult. One can introduce fine tubes into the oviduct from the uterus but otherwise the uterotubal junction in mares acts as a one-way valve preventing fluid ascent from the uterus. To some degree, this may explain the relative lack of oviduct pathology in mares compared to cattle.
Alter about six and a half days in the oviduct, incubating mainly at the ampullary-ithmic junction, embryos enter the uterus. In mares of course, single embryos are far more common than twin embryos. At that time, late morulas or early blastocysts can be collected by flushing the uterus. Before that time it is impossible to retrieve a fertilized embryo by flushing the uterus alone.
Although unfertilized oocytes are occasionally found in the uterus, this is unusual. In general, if an oocyte is not fertilized in mares, it will not reach uterus. This phenomenon is unique among equids. Therefore it is generally not important to determine if oocytes have been fertilized when they are collected for embryo transfer. It is now universally recognized that production of prostaglandin E2 by embryos (not oocytes) causes relaxation of oviduct smooth muscle. This allows transport of the embryo into the uterus. When mares are examined postmortem, it is not unusual to find flattened, degenerate oocytes from previous cycles, caught within the oviduct.
| Pathology? Fibrinous masses that can be several mm in size, are often found in the oviducts of mares. Again, this is a phenomenon peculiar to equids. It has been suggested that they are pathological and may block the passage of oocytes and embryos in the oviduct. However, these masses are found in 75% to 85% of mares (as reviewed by Tsutsumi, Y. 1979) therefore they are unlikely to be pathological. The origin of the masses is unknown but they may arise from fibrin discharged from follicles after ovulation, during the formation of corpora hemorrhagica. In that regard, it is also very common to see fibrin tags in and around the ovary in apparently normal mares. In fact, careful inspection of the images in this entry will reveal such tags. The author had the dubious privilege of spending many hours at an equine slaughter plant and saw such tags many times, often in young mares. The same can be said for para-ovarian (wolffian) cysts, sometimes reported as abnormal too. The vast majority of otherwise normal mares have these cysts. |
Selected references:
Allen, W.E. et al. 1979. Evaluation of uterine tube function in pony mares. Vet. Record 105: 364-366
Arnold, C.E. and Love, C.C. 2013. Laparoscopic evaluation of oviductal patency in the standing mare. Theriogenology 79: 905-910
Bennett, S. 2002. Surgical evaluation of oviduct disease and patency in the mare. Proc. AAEP 48:347-349
Betteridge, K.J. 2000. Comparative aspects of equine embryonic development. Anim. Reprod. Sci. 60: 691-702
Brinsko, S,P. 1991. The effect of uterine lavage performed four hours post insemination on pregnancy rate in mares. Theriogenology 35: 1111-1119
Dobrinski, I. et al. 1997. Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biol. Reprod. 56: 861-869
Freeman, D.A. 1991. Time of embryo transport through the mare oviduct. Theriogenology 36: 823-830
Ghazal, S et al. Glob. libr. women's med., (ISSN: 1756-2228) 2014; DOI 10.3843/GLOWM.10317
Hinrichs, K. 2010. In vitro production of equine embryos: State of the art. Reprod. Domestic Anim 45: 3-8
Hunter, R.H.F. 2008. Sperm release from oviduct epithelial binding is controlled hormonally by peri‐ovulatory graafian follicles. Molecular Reprod. Devel. Incorporating Gamete Research 75: 167-174
Inoue, Y. 2013 Hysteroscopic hydrotubation of the equine oviduct. Equine Vet J. 45:761-765
Kenney, R.M. 1993. A review of the pathology of the equine oviduct. R. M. Kenney. Equine Vet. J. 25 (S15): 42-46
Leemans, B.M. 2015. Why doesn’t conventional IVF work in the horse? The equine oviduct as a microenvironment for capacitation/fertilization. Reproduction 152: R233-R245
Navara, K. J. 2015. Higher rates of internal ovulations occur in broiler breeder hens treated with testosterone. Poult Sci. 94:1346-1352
Rigby, S. et al. 2000. Oviductal sperm numbers following proximal uterine horn or uterine body insemination. Proc. AAEP. 46:332-334
Saltiel, A. et al. 1986. Pathologic findings in the oviducts of mares. Am. J. Vet Res. 47: 594-597
Sieme, H. et al. 2003. The effects of different insemination regimes on fertility in mares. Theriogenology 60: 1153-1164
Smits, K et al. 2016 The equine embryo influences immune-related gene expression in the oviduct. Biol. Reprod. 36: 1-8
Tsutsumi, Y. 1979. Evidence of the origin of the gelatinous masses in the oviducts of mares.
J. Reprod. Fert. 57: 287-290
Weber, J.A. 1995. Relaxatory effect of prostaglandin E2 on circular smooth muscle isolated from the equine oviductal isthmus. Biol. Reprod. Monograph. series1: 125-130
