The Uterine Tube (Oviduct)

The uterine tube of the camelidae, as in other mammalian species, plays an important role in the storage of semen (sperm reservoir), fertilization and early embryo development (cf. Physiology). In guanacos (lama guanacoe), 20 to 25% of the sperm cells in the ejaculate are found at this level 120 hours after a single breeding.⁽⁹⁷⁾ The uterine tube is capable of these functions because of its peculiar macro and microscopic characteristics.
 

Macroanatomy

In the dromedary, the uterine tubes (tuba uterina) are long and tortuous. Their length ranges from 17 to 22 cm⁽⁷⁷⁾ or 25 to 28 cm.⁽⁸⁷⁾ They start with a wide abdominal end located close to the medial opening of the ovarian bursa and end in the corresponding uterine horn by a protruding utero-ovarian junction (isthmus or papillae) (Figure 5.35). The ampullary end is soft and flabby and presents a wide opening into the bursa. The uterine tube becomes harder and smaller in diameter and straightens before entering the isthmus region. The uterine-tube papillae are conical and protrude 2 to 5 millimeters into the uterine lumen (Figure 5.35).^{(77, 87, 96, 107)} The oviduct is covered by a fold of the peritoneum -the mesosalpinx - which is continuous with the broad ligament. The utero-ovarian artery runs parallel to the long axis of the oviduct within the mesosalpinx.⁽⁷⁷⁾

In the llama and alpaca, morphological features of the uterine tube are similar to those reported for the dromedary.⁽⁹⁵⁾ The length of the uterine tube is 10.5 cm in the llama⁽³⁸⁾ and 30.4 ± 4.2 cm in the alpaca.⁽¹³⁾

Histology

Complete histological study of the uterine tubes is available only for the dromedary camel.^{(71, 77)} The mucosa of the uterine tube is folded and fills most of the lumen. Mucosal folding is more pronounced in the ampullary region. The epithelial lining of the uterine tube is columnar and composed of ciliated and non-ciliated cells with oval or elongated nuclei. In some areas, tall narrow cells are observed in addition to normal epithelial cells. The subepithelial layer consists of loose connective tissue, blood vessels, lymphatics, and nerves. The tissue at the base of the folds is cellular and sometimes infiltrated with lymphocytes and contains some smooth muscle fibers. The lamina propria lies directly on a smooth muscle layer composed of an inner circular layer and an outer longitudinal layer. The circular smooth muscle layer increases in thickness from the ampullary region to the utero-tubal (isthmus) region where it forms a real sphincter (Figure 5.36, 5.37, 5.38).⁽⁷⁷⁾

Histological features of the uterine tube change according to ovarian activity.⁽⁷⁷⁾ In the presence of a mature follicle, the epithelium is tall columnar, predominately composed of ciliated cells with large elongated parabasal nuclei. During this early follicular phase, the subepithelial layer is infiltrated with lymphocytes. The connective tissue cells are small and blood vessels are scarce during this phase.⁽⁷⁷⁾ When a mature follicle is present, the subepithelial layer contains large connective tissue cells with a few lymphocytes and many congested vessels). The muscular fibers increase in size and the inner layer tends to be arranged into an inner oblique and a middle circular layer.⁽⁷⁷⁾

During the luteal phase, secretory activity is increased and the epithelium becomes tall columnar with equal incidence of ciliated and non-ciliated cells. The decrease in ciliated cells observed in the other species during the luteal phase or during pregnancy is not evident in the dromedary.⁽⁷¹⁾ Under the effect of progesterone, there is an increased blood supply to the subepithelium layer which becomes congested. The connective tissue is loose and edematous during the peak of the luteal phase. Regression of the corpus luteum is accompanied by a decrease in epithelium size. The epithelial lining becomes predominately ciliated with only a few cells showing secretory activity.⁽⁷⁷⁾ Both vascularization and size of the sub-epithelial layer decrease towards the end of the luteal phase. Lymphocytic infiltration is usually present at the base of some cells, within the lumen and the sub-epithelial layer.⁽⁷⁷⁾

During early pregnancy, histological appearance of the tubal mucosa is similar to that of the active luteal phase. The epithelial lining is tall columnar, composed of a mixed population of cells with elongated nuclei occupying different positions. Some cells show secretory projections while others are quiescent and ciliated. At mid-pregnancy, the secretory activity ceases and the sub-epithelial layer is vascular but infiltrated with lymphocytes.⁽⁷⁷⁾ At the end of pregnancy, the majority of epithelial cells are ciliated. Vascularization and hypertrophy of the connective tissue become more pronounced. Lymphocyte infiltration increases towards the end of pregnancy. The lumen of the uterine tube contains secretion mixed with epithelial cells and lymphocytes.⁽⁷⁷⁾

The ultrastructure of the surface of the uterine tube epithelium was studied by scanning electron microscopy.⁽⁷¹⁾ This study showed that cilia are uniform in length and evenly distributed. They usually extend above the apexes of the secretory cell processes and measure 0.2 µm in diameter and 5 µm in length. The epithelium is characterized by the presence of microvilli in both ciliated and secretory cells. These microvilli measure 0.2 to 0.6 µm in length and 0.2 µm in diameter.⁽⁷¹⁾ These ultrasstructural features confirm that the uterine tube is the site of both secretory and absorption activities. The dromedary uterine tube infundibulum, like that of other ruminants, consists essentially of ciliated cells. Ciliated cells are widely distributed during the follicular phase and probably play an important role in the Pansport of the ovum.⁽⁷¹⁾ The secretion activity is of the apocrine type, increases during the follicular and luteal phases, and probably has an important role in promoting the fertilization process and early embryo development.⁽⁷¹⁾ Fertilization takes place in the lower third of the uterine tube and the embryo develops in this organ for the first 5 days after fertilization, reaching the uterus as a recently hatched blastocyst.

The uterotubal junction

The uterine end of the oviduct (isthmus) is quite peculiar in camelidae in that it is well developed (Isthmus tubae uterime). The intramural part of the uterine tube measures 11-14 mm in length and 3-4 mm in diameter. The uterine tube extends into the uterine cavity by a conical or pyramidal papilla (Papilla uterina tubae uterime) measuring 2 to 5 mm in length and 1 to 2 mm in diameter. The papillae are very muscular and present a sphincter muscle at its apex (Figure 5.38). The reason for this peculiarity has not been fully investigated. It is possible that the papilla plays an important role in the selective transport of fertilized embryos.

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