Fertilization and Pregnancy

Oocyte maturation and fertilization

The process of fertilization has not been studied in the camelidae. It is likely that in order for this process to be completed, as in many other mammals, two main conditions have to be fulfilled -namely oocyte maturation, and sperm capacitation and acrosome reaction. There are no studies available on these processes in the camelidae. Because of the induced nature of ovulation in these species, it is likely that oocyte maturation is completed during the phase immediately following copulation and LH release and shortly after ovulation. Collection of oocytes from pre-ovulatory follicles at different times after hCG injection or sterile mating shows that as ovulation time approaches, the cumulus-oocyte complex (COC) displays changes similar to those described in pre-ovulatory COC in other species, especially expansion of the cumulus cells (Figure 6.10). Cumulus dispersion is observed in COC recovered by aspiration from follicles 18 to 24 hours after hCG injection. Ovulation usually takes place 24 to 48 hours after breeding in camels and llamas. It is possible that this time allows for the final maturation of the oocyte and its release following the peak of LH which begins 2 hours after copulation.

No detailed studies are available on capacitation and acrosome reaction in camelidae spermatozoa. However, given the morphology of the spermatozoa which is very similar to that of other domestic mammalians, this process should be very close to those reported in other mammals. The period required for sperm capacitation and acrosome reaction to be completed is unknown in the camelidae, but since ovulation does not usually occur in these species until 24 to 48 hours after insemination or breeding, one can speculate that sperm has matured and remains viable at least during this time lapse. The site of semen deposition after breeding varies according to studies. In the llama and alpaca, the site of semen deposition is considered to be intra-uterine with semen deposited equally in both horns.⁽⁵²⁾ In the dromedary, many authors have suggested that semen is deposited inside the uterine cavity; however, serial fibroscopic and ultrasonographic examinations of the cervix and uterus in our laboratory indicate that semen is deposited in part in the anterior vagina, and in part in the cervical canal and the uterus. There is no forceful ejaculation in camelidae. Semen is dribbled continuously during intercourse, first in the vaginal cavity and then, as the penis is threaded into the cervical rings, more semen is deposited in the cervical canal and the internal cervical os. Shortly after ejaculation, sperm cells are transported (probably by uterine contractions which are at their maximum during the period of receptivity) to the utero-tubal junction which acts as a sperm reservoir in camelidae.⁽²¹⁾ In the guanaco, as much as 20 to 25% of the ejaculated sperm cells are found in this area up to 120 hours after breeding.⁽²³⁴⁾ In the llama, sperm cells stored in the isthmus (utero-tubal junction) can remain viable up to 5 days.⁽²⁵²⁾ We have been able to collect highly motile spermatozoa from the oviduct of dromedary camels up to 3 days following mating. It is possible that sperm cells are released progressively from this site of storage to guarantee fertilization when the oocyte is shed and transported into the uterine tube. After ovulation, the ovum is picked up by the fimbria of the large infundibulum and carried to the site of fertilization (the uterine tube) where the initial stages of embryo development are found.
 

Fertilization rate in the alpaca ranges from 66.6 to 85.7% and is higher for left ovulations (100%) than for right ovulations (81%) though this difference is not statistically significant.⁽¹¹³⁾ In the controlled breeding program that we conduct in the dromedary, breeding is done on the basis of the presence of a mature follicle (10 to 18 mm) and increased uterine tone. The resulting fertilization rate is 81.4%.⁽²⁵³⁾ Fertilization rates are respectively 82.3% and 83.9% for single and double ovulations. When breeding is based on estrus detection, the highest conception rate (50%) is achieved when female dromedaries are bred on the first or the second day of estrus and the lowest (14.3%) when they are bred on the fifth day of estrus.⁽¹²⁷⁾ The cumulative conception rate is 100% when females are bred every 24 hours during the first 3 days of estrus, and only 62.5% to 75% when females are bred on the third day of estrus and beyond.⁽¹²⁷⁾

Little information is available on the chronology of embryo segmentation in the dromedary. Our embryo collection results (cf. Embryo Transfer) suggest that the development of the embryo from one cell to a hatched blastocyst takes 6.5 to 7.5 days. All early stages of embryo segmentation take place in the uterine tube, because collection of dromedary and llama embryos from the uterus yields mainly hatched embryos or embryos in the process of hatching (Figure 6.11 ).^{(7, 25, 47, 159)} The process of hatching seems to be very fast in these species.

In the llama, flushing of the uterine tubes at regular intervals from breeding yielded 1- to 2-cell embryos, 4- to 8-cell embryos, 8- to 16-cell embryos and morula at 48 hours, 72 hours, 96 hours and 96 hours respectively.⁽²⁰⁶⁾ It is interesting to note that in the same study, 17 eggs were collected from 9 animals and 6 of these eggs were non-segmented.⁽²⁰⁶⁾ In the alpaca, it was reported that the embryo reaches the uterine cavity 3 days after ovulation.⁽¹²¹⁾

Embryo transport through the uterine tube and especially through the utero-ovarian junction into the uterus seems to be under the influence of the embryo. Our results of uterine flushing in females after sterile mating suggests that the non-fertilized oocyte does not reach the uterus after ovulation (cf. Embryo transfer). It is possible that the camelidae are similar to horses with respect to oviductal transport of the embryo. In the equine, embryo transport through the oviduct is regulated by prostaglandin E 2 (PGE2).⁽²⁵⁴⁾

Embryo fixation and implantation

Descent of the embryo into the uterus occurs between day 6 and day 7 after ovulation in the dromedary.^{(125, 159)} and 3 to 4 days after ovulation in the llama and alpaca.⁽¹²¹⁾ At this stage, the embryo is hatched or is in the process of completing its hatching from the zona pellucida. The freshly-hatched embryo is usually spherical and shows a dense spot corresponding to the embryonic cell mass (Figure 6.11). The embryo expands rapidly, loses it spherical shape between day 9 and 10 post-breeding, and starts to elongate. Elongation of the embryo has been reported in the dromedary and Bactrian camel at day 15 following mating.^{(221, 222)} Its dimensions are 2.2 x 1.8 mm. The external cellular layer of the trophoblast is uniformly distributed. Flat endoderm cells are situated below except at the site of the dense embryonic node. The latter is not lined with endoderm. The embryonic mass is dense and slightly elongated. Elongation of the early embryo in the camelidae is a very important feature because it gives an insight on the mechanism of pregnancy recognition in these species. Maternal recognition is a very important physiological phenomenon that allows the maintenance of the corpus luteum by preventing the uterus from releasing prostaglandin F2α and causing luteolysis. In most domestic species the signal for blocking the PGF2α release is given by the embryo either through migration (mobility), as in the case of horses, or by elongation, as in the case of ruminants. It is likely that the second mechanism prevails in camelids since elongation of the embryo coincides with the time of the demise of the corpus luteum and fall of progesterone in the case of non-fertile mating (day 10-11).
 

After the period of elongation, the conceptus becomes fixed and starts to develop close attachments with the uterus (implantation). Fixation of the embryo seems to take place around day 20 post-ovulation.⁽²²²⁾ The time of embryo implantation is not well-defined in camelidae. It is assumed that the conceptus remains free within the uterus for the first 30 days of its life because no firm attachment between the trophoblast and the uterine wall is observed at this time in the alpaca.⁽⁶³⁾ Also, this period (30 days of pregnancy) is characterized by a high incidence of early embryonic death which confirms that the conceptus is not fully attached and is still very sensitive.^{(113, 206)} At 60 days, however, the placenta is usually well-developed and shows a vascular connection with the uterus. Full attachment between the placenta and the uterine mucosa is completed between 60 and 90 days of pregnancy.⁽⁶³⁾ Based on the morphology (fetal heart beats) and estrone sulfate profiles, it is suggested that implantation in the alpaca and llama begins around days 20 to 22 post-breeding.⁽⁶⁰⁾

In the dromedary, hysteroscopy clearly shows that the elongation process of the embryo starts before day 20. The conceptus extends to occupy the lumen of the left uterine horn between days 20 and 25 and the right uterine horn between days 25 and 35.⁽²²⁶⁾ Uterine embryo flushing at different times post-breeding shows that the embryo loses its spherical shape around day 10 (collapsed) and starts to elongate to reach a length of 8 to 12 cm by day 15 (Anouassi and Tibary, unpublished) (Figure 6.13). This considerable elongation of the dromedary conceptus facilitates the close contact between the endometrium and the trophoblast, and the formation of a microvillous attachment between the allantochorion and endometrial epithelium which constitutes the final implantation and placentation. The implantation of the dromedary embryo probably occurs around 50 days because at this stage the fetus is attached to the ventro-medial or ventro-lateral uterine wall by a short yolk stalk which later becomes the umbilical cord.^{(224, 226)}

One of the major peculiarities of embryo fixation and pregnancy in camelids is that nearly all pregnancies are located in the left horn.^{(60, 104, 111-114, 119, 128, 171, 215, 249, 250)} This siuiatipn predominates (98 to 100%) in all camelidae although the corpus luteum's location is equall) distributed between the left and right ovary. A higher incidence of right-horn pregnancies was reported in only one study in the dromedary.⁽¹³⁴⁾ These authors reported an incidence of 30 to 60% of right-horn pregnancies even for stages ol pregnancy beyond 95 days. The discrepancy between the results of this particular study and those of all other published studies on this topic raises some doubt as to their validity.

In the llama and alpaca, in spite of both ovaries being equally active (as evidenced by equal distribution of active corpora lutea in the right and left ovaries), 98.4% of a total of 928 pregnancies in alpacas were carried in the left uterine horn. The pregnancy was supported by corpora lutea located in the right ovaries in 50.4% of the cases.^{(118, 119)} These observations indicate the need for embryos originating from ovulations in the right ovary to migrate to the left uterine horn in order to survive. In another study on alpacas, only one fetus out of forty eight (2%) was located in the right uterine horn at 120 days of pregnancy.⁽⁶⁰⁾

This predisposition of left-horn pregnancies in camelids has been initially attributed to a difference in activity between the left and right ovary or by the difference in size between the left and right horn. Although some authors have suggested that the left ovary is more active than the right one, our observations and those of others confirm that the two ovaries are equally active and therefore, side of ovulation is not the primary cause of left-horn pregnancy (Table 9). In addition, results from our embryo-transfer experiments show that pregnancy is maintained with equal frequency whether the recipient has a corpus luteum on the left or on the right ovary. Also, all embryos deposited into the right horn migrated to the left horn after a few days. During our routine ultrasonographic pregnancy diagnosis at 15 to 18 days post-breeding, nearly all embryonic vesicles were detected in the left horn. In fact, out of 1248 pregnancy diagnoses by ultrasonography at this stage we detected an embryonic vesicle in the right horn only thrice. Therefore, there is definitely an embryo migration from the right uterine horn to the left horn when ovulation occurs on the right ovary. It is highly likely that in order for a corpus luteum to be maintained the conceptus has to send a signal directly to the left horn in order to prevent PGF2α release. Following this theory, it is possible that pregnancies where the embryo fixation occurs in the right horn result in a higher early embryonic death and therefore are rarely detected.
 

Migration of the conceptus is justified by the difference in luteolytic effect existing between the left and right uterine horn.⁽¹¹⁴⁾ PGF2α release from the right uterine horn is local whereas PGF2α from the left horn is released into the main blood stream and can reach and cause luteolysis in the right as well as the left ovary. The migration of the embryo originating from an ovulation in the right ovary to the left horn is therefore required to prevent PGF2α release into the general circulation and may even exert a luteotropic effect making the survival of the embryo possible.^{(114, 118)}

The exact mechanism of embryo migration is not known. It is possible that embryo migration from the right to the left horn is simply due to a physical property of the left horn, which is larger than the right horn, to better accommodate the expanding embryo. It has also been suggested that this migration is facilitated by the shortness of the uterine body, the smallness of the right horn and the increased number of mucosal folds in the endometrium of the right horn.^{(175, 176)} This theory is supported by the fact that the discrepancy in size between the left and right uterine horns exists in prepubertal animals and even during fetal stages (cf. Anatomy). This difference in size increases with the number of pregnancies.^{(175, 176)} Mobility of the embryo as observed in the mare is less likely to happen in camelids, because of the decrease in tone and contraction of the uterus during pregnancy.

Placentation and fetal growth

Development of the feto-placental unit is usually divided into 3 periods: the period of the ovum, the period of the embryo and the period of the fetus.

Period of the ovum

The period of the ovum is the time from fertilization until hatching. In camelidae all these stages of development take place in the uterine tube.

Period of the embryo

This period is defined as the development stage from descent of the embryo into the uterus until implantation. The embryo sheds its zona pellucida and enters the uterus around day 6.5 to 7 post-breeding in both the dromedary and Bactrian camels, at day 3-4 in alpacas,⁽¹²¹⁾ and at day 6 to 7 in the llama.^{(7, 47, 265)} Elongation and formation of a trophoblastic vesicle starts at 14 days. The conceptus takes on the appearance of a tube.^{(175, 179, 180, 209, 221, 222)}

The development of the provisional organs - the amnion, yolk sac, and allantois - shows some peculiarities. The amnion is laid down when the embryo has more than 10 somites which is later than cattle and sheep. The yolk sac has no central swelling. Organogenesis presents the same features observed in the other ungulates. At the stages of formation of the visceral fissures and arches, the embryo has a small liver and mesonephros. The heart beats are present by day 22 of pregnancy. Differentiation of the major organs is completed between 45 and 60 days of pregnancy.^{(175, 179, 180, 209, 221, 222)}

Period of the fetus

The period of the fetus is the time from implantation until parturition. It is characterized by a steady increase in uterine size allowing accommodation of the developing fetus and its membranes and fluids.

Growth of the uterus

During pregnancy, the dromedary's left horn develops first with right-horn development lagging far behind. During the first 6 weeks of pregnancy most of the uterine growth concerns the greater curvature of the left hom (Figure 6.14). The growth in the right greater curvature of the uterus starts to be significant at about 100 days of pregnancy. Growth of the lesser curvature becomes significant around 150 days of pregnancy.^{(171, 179)} The circumference of the right horn starts to increase after 2 months of pregnancy. The size of the left hom is similar to that of the right hom during the first month of pregnancy but becomes twice the size of the right horn at 3 months (Figure 6.14). The thickness of the uterine wall remains constant throughout the gestation period. Most of the weight of the pregnant uterus is due to the weight of the uterine tissue itself during the first 2 months of pregnancy. From two months until 225 days of pregnancy, most of the weight of the uterus is due to increased placental tissue and amount of fetal fluid which increases from 2 liters at 90 days to 9 liters at 225 days.⁽¹⁰⁴⁾ The majority (80 to 90%) of the fetal fluid is allantoic in both the dromedary⁽¹⁸¹⁾ and the Bactrian camel.⁽⁶⁹⁾

The Placenta

Placentation in camelidae is diffuse epitheliochorial, similar to that of the equine species.^{(37, 68, 122, 124, 128, 162, 166, 186, 191, 258, 259)} The allanto-amnion and allanto-chorion are arranged similarly to those of the bovine.⁽¹²⁸⁾ There is an adhesion between the allanto-amnion and the alantochorion along the whole dorsal surface of the pregnant hom. As a result, the allantoic cavity is restricted to a wide channel which runs along the ventral side of the pregnant horn. The amniotic sac containing amniotic fluid is seen during the first month of pregnancy. The amniotic cavity becomes very small compared to the allantoic cavity as pregnancy advances. The amniotic membranes are never seen in the non-pregnant horn.^{(179, 181)}

An extra-fetal membrane, called the epidermal membrane, epithelion, or 4th membrane, is found in all species of camelidae.^{(122, 161, 174, 279)} This membrane is made up of a layer of epithelial cells that cover the entire fetus. It is connected to the mucocutaneous junction of the lips, nose, eyes, and coronary bands (Figure 6.15) (cf. Anatomy of the placenta). It is not exactly known when this membrane first appears but in the dromedary it can be easily identified at 3 months of gestation.⁽¹³⁴⁾ Due to the presence of this membrane, the fetus is never directly in contact with the amniotic fluid, unlike in other domestic animals. The epidermal membrane is thought to play an important role as a lubricant during parturition because of its slippery nature, as well as protection from dehydration for the newborn. In the dromedary, we have noticed that once the newborn stands, this membrane is shed along with all the sand that has collected over the body after birth.

The size and diameter of the umbilical cord increases with advancing gestation. The cord of the dromedary fetus at full term measures 45 to 50 cm and is usually twisted clockwise.⁽¹³⁴⁾

Morphological change in the fetus

Development of the fetus throughout pregnancy was thoroughly investigated in the dromedary⁽¹⁰⁴⁾ and in the alpaca.^{(60, 231)} These studies led to the development of a prediction equation for pregnancy stage based on different measurements taken on the fetus. The same studies also give detailed accounts of the morphological changes of the conceptus throughout pregnancy. This information is critical for the veterinary practitioner to determine the stage of pregnancy based on morphology of the fetus in the case of abortion. In all species of camelidae, fetal growth rate is very slow during the first 6 months of pregnancy then increases in the last trimester. In fact, 65% of the fetal weight increase occurs during the last 3 months of pregnancy.^{(60, 104)} During the last four months (270 to 390 days) the fetus is the major contributor to the total mass of the gravid uterus.^{(60, 104)} In the dromedary, fetal weight doubles during the last 45 days of pregnancy.⁽¹⁰⁴⁾
 

In the alpaca and llama, 85% of the weight gain occurs from 210 days until parturition. Fetal weight of alpacas at 8 months, 9 months and 10 months of gestation is respectively 30%, 51% and 65% of that at birth. At 11 months, fetal weight (8.6 kg) is not significantly different from weight at birth (8.8 kg).⁽⁶⁰⁾ Morphogenesis is completed by 60 days of pregnancy. Macroscopic fetal sex determination is not possible at 30 days but is easy at 60 days.⁽⁶⁰⁾ The presence of hair on the lips, eyebrows, and tail is observed at 7 months of gestation, and the body is completely covered by hair by 8 months of gestation.^{(60, 67)}

Several equations were elaborated for the estimation of gestation stage from measurements taken on the fetus (Table 10). The highly significant coefficients of correlation between gestation age and body measurements indicate that prediction of the fetal age is possible with a fair degree of accuracy using the above regression equations. However, the accuracy of the determination might be improved by using more than one equation and averaging the results. This method certainly eliminates the possibility of being misled by an extreme variation in one dimension.^{(104, 134)}

Fetal presentation within the uterus shifts from being predominately posterior in early gestation to anterior with advancing stages of pregnancy. At the end of pregnancy, almost all fetuses are in an anterior presentation.⁽¹⁷⁵⁾ The fetus is lying on the right side or the left side in equal frequency from early development until mid-pregnancy. After this, the majority of the fetuses are lying on the right side.⁽¹⁷⁵⁾ During early fetal development, the posture is such that the whole fetus is curved with the legs extended under the body. From 2 to 2.5 months, the body and the neck of the fetus are extended. The posture of the fetus remains the same from mid-pregnancy until term. The body and the neck are extended. The head is slightly flexed at the occipital joint. The fore and hind limbs are flexed under the body.⁽¹⁷⁵⁾
 

Y= pregnancy stage in days
X = measurement taken on the fetus in cm for length or in kg for weight
 

Endocrinology of pregnancy

The study of endocrinology of pregnancy in any species is very important in that it can help understand the mechanisms of pregnancy recognition, pregnancy loss, and the fine tuning between the feto-placental unit and the uterus which lead to a normal parturition. There are several hormones involved, with variable degrees of intensity during pregnancy, in the maintenance of viability of the fetus, growth of the uterus, and the preparation of the latter for the final event of parturition. These hormones include estrogens, progesterone, relaxin, prostaglandin, and thyroid hormones (Figure 6.16). The origin of the hormones encountered during pregnancy can be maternal (such as progesterone from the ovary), fetal (such as ACTH), or placental (such as estrogen).
 

Estrogen

Estrogen levels increase by day 18 to 20 after mating and show a great variation during the first two trimesters of pregnancy. Estradiol-17ß starts to increase around 20 to 25 days post ovulation in the dromedary and reaches a peak of 100 pg /ml by 60 to 70 days.⁽²²⁹⁾ Some authors attribute this initial rise in estrogen to ovarian follicular activity.^{(94, 95, 180)} This is justified by the fact that follicular activity in the dromedary is not inhibited until 6 months of pregnancy.^{(104, 124, 180, 212)} However, mature follicles (< 10 mm) are generally not found beyond 105 days of pregnancy.^{(104, 124)} The main source of estrogen -especially estradiol-17ß - in early pregnancy is the embryonic vesicle or the placenta. This is supported by the high aromatizing ability of the extra embryonic membrane, which is present as early as 10 days post-fertilization, as well as to the capacity of the dromedary endometrium to conjugate free estrogen.⁽²²⁵⁾ Conjugated estrogens are found in high levels in maternal blood in the form of estrone sulfate. The feto-placental origin of estrogen in the pregnant dromedary is also demonstrated by the sharp fall of the concentration of this hormone after expulsion of the fetus and placenta following abortion or parturition.^{(17, 229)} Estrogen levels are also very high (2411 ± 390 pg/ml) in the allantoic fluid at parturition.^{(84, 94, 95)} The increase in estrogen in the maternal blood and allantoic fluid found during the last month of pregnancy could be due to an increased conversion of 17ß-hydroxyprogesterone to estrogen through a 17ß-hydroxylase system.⁽²²⁹⁾

Estrogen remains elevated throughout the pregnancy in the dromedary, ^{(17, 84, 85, 94, 95, 103, 229)} then decreases rapidly after expulsion of the fetus and placenta.⁽²²⁹⁾ Estradiol increases steadily to reach a peak during the last trimester of pregnancy.^{(15, 17, 84, 94, 103, 229)} Estradiol-17ß concentrations increase progressively during pregnancy from a basal concentration of 20 pg/ml at 2-3 months of pregnancy to about 450 pg/ml during the final stage of gestation.⁽¹⁷⁾ A dramatic increase in estradiol-17ß concentrations is seen between 10 months (338 pg/ml) and 12 months (606 pg/ml) of pregnancy.⁽⁹⁴⁾ The timing of estrogen increase in the pregnant dromedary coincides with the important period of increase in fetal weight and fetal fluid volume between 9 and 12.5 months.⁽¹⁰⁴⁾ Concentration of estrogen increases during the last 4 to 5 days before parturition.⁽⁹¹⁾

The marked increase in estrogen levels in the maternal blood observed after day 300 of pregnancy in the dromedary ^{(94, 229)} is accompanied by a decrease of progesterone and leads to a change in the ratio of estrogen to progesterone in favor of the former which is probably necessary for the preparation of the uterus for a normal parturition. Without this change, normal softening of the cervix and the ability of the uterus to contract during parturition are severely impaired. Although spontaneous parturition is possible even when animals are receiving exogenous progesterone,⁽²²³⁾ we found that many animals may experience insufficient cervical dilation and uterine contraction (Anouassi and Tibary, work in progress).

Estrogen profile during pregnancy in llamas and alpacas is similar to that described for the dromedary.^{(56, 149)} In these species, estrone sulfate concentration remains basal during the first 17 days of pregnancy then increases rapidly between days 21 and 25, probably as a result of the aromatizing activity of the trophoblast. Another increase is seen from the 11th month of pregnancy until delivery.^{(49, 56)} In the pregnant llama, estradiol-17ß is at basal concentration (10-46 pg/ml) during the majority of pregnancy and does not peak (196 ± 10 pg/ml) until the final third of pregnancy.⁽¹⁴⁹⁾ During the first 9 months of pregnancy, the combined estrone + estradiol-17ß and estradiol-17ß concentrations range between 6 and 274 pg/ml and 4 and 114 pg/ml respectively. After the 9th month of pregnancy these levels increase to peak at 827 ± 58 pg/ml for estrone + estradiol-17ß and 196 ± 10 pg/ml for estradiol-17ß during the last week of pregnancy.⁽¹⁴⁹⁾

In the Bactrian camel, detailed studies on the endocrinology of pregnancy are lacking. In one study, limited to the last month before parturition, estradiol-17ß was high (30 ng/ml). A further increase was observed 3 days before parturition, peaking at 55 ng/ml on the day of delivery and declining within the first 4 days postpartum.⁽²⁸³⁾

Progesterone

Studies on progesterone level during pregnancy in the camelidae confirm that these species depend on ovarian progesterone throughout their pregnancy. During pregnancy, progesterone levels in all species of camelids remain above 2 ng/ml from the initial detection with corpus luteum (CL) formation until shortly before parturition. Also, ablation of the CL-bearing ovary or administration of a luteolytic dose of PGF2α or its analogue causes abortion or premature parturition at all stages of pregnancy.⁽²³⁸⁾ (Tibary and Anouassi, unpublished) (cf. Hormone therapy).

In the dromedary, serum progesterone concentrations increase and reach levels greater than 2 ng/ml 6 days after ovulation.⁽¹⁵⁶⁾ Progesterone levels are identical for pregnant and non-pregnant females until 8 days post ovulation, after which they decrease rapidly to basal levels in non-pregnant females and are maintained above 2 ng/ml in pregnant females.⁽¹⁵⁶⁾ During the first month after mating, progesterone levels show a considerable individual variation and range from 3 to 9 ng/ml.^{(15, 17, 19, 95, 156)} According to some studies, progesterone levels in the dromedary decrease gradually from 5 months of gestation until parturition.⁽⁹⁵⁾ Others found that the mean progesterone concentration was slightly higher during early pregnancy and fluctuated between 4 and 5.5 ng/ml throughout gestation with the exception of a mild decrease between the ninth and tenth months of pregnancy.⁽¹⁵⁾ In a recent report, progesterone levels during the first 90 to 100 days were relatively constant (3 to 5 ng/ml), then decreased significantly to stabilize for the rest of the pregnancy at 2 to 4 ng/ml.⁽²²⁹⁾

The decrease in plasma progesterone reported after 3 months⁽²²⁹⁾ or after 5 months⁽⁹⁵⁾ cannot be easily explained. The rate of progesterone secretion should normally be constant since there is no change in the size of the corpus luteum of pregnancy after 60 days.⁽¹⁰⁴⁾ However, earlier studies showed a gradual decrease of lipid content in the luteal cells and an increase of connective tissue elements in the CL as pregnancy advanced. Even though the CL persists at nearly the same size and weight throughout gestation its secretory activity may decrease.⁽²⁴⁹⁾ A more logical explanation    of this observed decrease in concentration of progesterone would be through an increase of total blood volume. Other factors have been found to affect the level of circulating progesterone in the pregnant female dromedary. These include the sex of the fetus and age of the dam. Levels in camels bearing a male fetus are significantly higher than those carrying a female fetus (5.1 ± 0.6 vs. 3.6 ± 0.3 ng/ml).⁽¹⁵⁾ Mean plasma progesterone concentrations are 2.2 ± 0.3 ng/ml, 5.56 ± 0.71 ng/ml and 3.9 ± 0.3 ng/ml for females 5 years or younger, 5 to 10 years old and 10 years and older, respectively.⁽¹⁵⁾ The biological significance and practical value, if any, of these variations is not known.

In the llama and alpaca, the first increase in plasma progesterone is observed by day 3 to 4 following mating. Progesterone secretion by the corpus luteum becomes significant 5 days after mating as evidenced by the increase in levels of this hormone in the plasma and its metabolite in the urine.^{(49, 56, 149)} Levels of plasma progesterone remain above 2.0 ng/ml (3 to 4.5 ng/ml) throughout most of pregnancy. These levels of progesterone are positively correlated with the size of the corpus luteum in these species.^{(8, 12, 111)} A transient decrease in progesterone was described between days 8 and 10 in pregnant llamas^{(8, 12)} and at day 13 in alpacas.⁽¹¹¹⁾ This stage corresponds to the stage for release of PGF2α in non-pregnant females and of expansion of the conceptus that prevents luteolysis. Alpacas have substantial serum concentrations of 20α-dihydroprogesterone in addition to progesterone.⁽¹¹¹⁾ The physiological importance of this progesterone metabolite in the llama is not known. A slight decrease in progesterone plasma level is observed between 18 and 27 weeks.⁽¹⁴⁹⁾

In the llama, pregnancy is always associated with high plasma progesterone concentrations, between 5 and 9 ng/ml in the last month.^{(8, 235, 236, 245)} Similarly, in alpacas, progesterone levels remain above 2 ng/ml until the last month of pregnancy.^{(49. 52. 55, 111, 112)} Progesterone starts to decline about 2 weeks before parturition, drops markedly during the final 24 h before parturition, and returns to basal concentrations (<0.5 ng/ml) by the day of parturition.⁽¹⁴⁹⁾ Similar decline is found in the urinary metabolite of progesterone (pregnanediol glucoronide) during the last 5 days of pregnancy. ⁽⁵⁶⁾ However, complete disappearance of progesterone does not occur prior to delivery.^{(56, 149)} The regulatory mechanism(s) associated with the gradual decline in progesterone concentrations during the last 2 weeks before parturition is unknown and could be due to the conversion of progesterone to estrogen by 17-hydroxylase, synthesized in response to fetal cortisol secretion. This change in the estrogen-to-progesterone ratio could be important for the promotion of myometrial activity by increased synthesis of gap junctions and contractile proteins.

Thyroid hormones

Thyroid hormones play an important role in modulating metabolic activity, growth, and differentiation of vital organs.⁽¹⁸⁾ The average peripheral concentrations of T4 and T3 in pregnant dromedaries varies from 75.9 to 116.2 ng/ml and from 0.73 to 1.32 ng/ml, respectively. These values are similar to those reported for male camels.^{(16, 18)} Thyroid hormones are at their highest level between 2 and 5 months and lowest between 8 and 10 months of gestation.⁽¹⁸⁾ Thyroid activity increases during the last stage of pregnancy in dromedaries.^{(16, 273)} This fluctuation in thyroid activity may be due to variation of other hormones, especially estrogen and progesterone, during pregnancy.⁽¹⁶⁾ Since gestation length in the camel is about one year, climatic factors may also contribute to these fluctuations, as seasonal effects on plasma thyroid hormones in the camel have been documented.⁽¹⁶⁾ Some thyrotrophic hormone-like activity in the camel placenta has been detected during the second half of gestation.⁽⁴⁾ Increased thyroid activity during pregnancy is probably necessary for a better utilization of the nitrogen metabolic pool to meet the requirements of the tissues of the reproductive system and of the growing fetus.⁽¹³⁰⁾

In the llama, plasma triiodothyronine concentrations vary between 0.5 and 4.5 ng/ml (1.9 ± 0.1) throughout pregnancy and the peri-parturient period.^{(149, 230)} Plasma thyroxine concentration varies between 21.3 and 91.5 ng/ml (56.5 ± 0.8) from mating until about 39 weeks of pregnancy when it begins to decline, and falls from 43.0 ± 5.3 ng/ml at 15 days pre-partum to 23.5  ± 5.5 ng/ml immediately before parturition. The concentration increases to 52.8 ± 3.9 ng/ml by 1 day postpartum.⁽¹⁴⁹⁾ The decline in thyroxine during the last weeks of pregnancy could be the result of nutrient redistribution to the mammary gland in preparation for lactation.⁽¹⁴⁹⁾

Other hormones

Is there a camelid chorionic gonadotropin?

The presence in the dromedary of a chorionic gonadotropin with high FSH and/or LH activity, such as that found in the pregnant mare, has been suggested by some authors as a mechanism for the emergence of secondary corpora lutea.^{(90, 132)} The presence of such a hormone with high FSH activity is based on ovarian response in mice injected with serum from pregnant camels carrying fetuses with a CRL of 11 to 58 cm.⁽⁹⁰⁾ Another study suggested the presence of such a chorionic hormone based on a mouse Leydig cell bioassay for LH activity (production of testosterone) and rat granulosa cell FSH bioassay (production of estradiol-17ß).⁽¹³²⁾ These findings led the authors to suggest that there are two sets of corpora lutea during pregnancy in the dromedary: primary and secondary corpora lutea. The secondary CL supposedly develops after 70 days of pregnancy.⁽¹³²⁾ Our observations on corpus luteum function during pregnancy by ultrasonography and measurement of progesterone levels for hundreds of pregnancy diagnoses do not support this theory of the presence of a secondary corpora lutea. Also, recent trials, using modem laboratory techniques, have failed to demonstrate this chorionic gonadotropin in dromedaries (Sghiri A. & Combarnous, personal communication).

Prostaglandins

In the dromedary, secretion of prostaglandin F2 alpha (PGF2α), as revealed by measurement of its metabolites (PGFM), is inhibited during pregnancy until 50 days prior to parturition where an increase in PGFM is noticed parallel to the increase in estrogen.^{(91, 229)} A sharp peak of this hormone occurs on the day of parturition.^{(91, 229)}

Relaxin

In the alpaca, relaxin remains at its basal levels during the first months of pregnancy then increases significantly at 3.5 months. A decrease in this hormone is observed between 5.5 and 7 months of pregnancy followed by a steady increase until parturition. Relaxin is probably secreted by the feto-placental unit and is implicated in the growth of the uterus during pregnancy and relaxation of the ligaments and cervix at the end of pregnancy.⁽⁵⁰⁾

The corpus luteum of pregnancy

The corpus luteum of pregnancy presents several morphological characteristics. It constitutes the major source of progesterone during pregnancy in the camelidae and is present until delivery.^{(12, 100, 212, 238)}

Corpus luteum presence is mandatory for the maintenance of pregnancy in camelidae. Removal of the conceptus or administration of PGF2α causes a regression of the CL in 5.5 days on the average (range 4 to 7 days) in llamas.⁽⁴⁶⁾ Administration of luteolytic doses of PGF2α or its analogues or surgical ablation of the corpus luteum results in abortion if done before the 10th month of pregnancy and in premature birth if done later.^{(232, 238, 240)} In the dromedary, abortion or parturition usually occurs between 8 and 72 hours after injection of PGF2α or its analogue (cf. Hormone Therapy in camelidae).

In the dromedary, the corpus luteum of pregnancy is almost spherical with a liver-like consistency and an orange or reddish color.^{(98, 100, 101)} It protrudes from the surface of the ovary and shows blood vessels on its surface (cf. Anatomy). The size, position, and form of the CL are subject to high individual variations during pregnancy.^{(184, 212, 253)} In early pregnancy the CL has a flabby consistency, and is sometimes cavitary, becoming larger and firmer as gestation advances.⁽²⁵³⁾ Enucleation of corpora lutea is very difficult and should never be attempted because of the high risk of trauma and development of adhesions.⁽¹⁰⁴⁾ The section of the coipus luteum shows a thin whitish capsule of about 1 mm thickness in the middle of dark-reddish-brown luteal tissue (Figure 6.17). The diameter of the CL varies but it is generally greater than 2 cm.^{(100, 220, 253)} On the average, the CL of pregnancy measures 22.3 mm in length and 21.5 mm in width.⁽²²⁰⁾ Based on rectal palpation and ultrasonography, the major increase in corpus luteum size occurs during the first 2 months of pregnancy.^{(104, 253)} Ultrasonographic observation of the corpus luteum during the first 90 days of pregnancy shows that its diameter increases during the first 25 to 30 days then stabilizes at around 22 mm.⁽²⁵³⁾ Many corpora lutea show a central anechoic cavity which becomes more dense and filled with luteal tissue as gestation advances. In general, cavitary corpora lutea are a lot larger in diameter that a non-cavitary CL.⁽²⁵³⁾  The individual size of the corpus luteum of pregnancy is sometimes smaller (15 to 18 mm) when two or more corpora lutea are present, especially when they are located on the same ovary.⁽²⁵³⁾

Presence of 2 to 4 corpora lutea on the same ovary or distributed between the left and right ovary is not a rare occurrence (Table 11). In the same female, incidence of multiple corpora lutea ranges from 10 to 20%.^{(98, 100, 104, 253)} Some authors suggest that the presence of multiple corpora lutea during pregnancy is due to secretion of a chorionic gonadotropin (see above) which is responsible for the development of "secondary corpora lutea" as seen in the mare. We refute this theory on the basis that only a fraction of pregnant animals have multiple corpora lutea. Also, we have failed to identify any newly-formed corpora lutea in pregnant animals by weekly examination until 100 days of pregnancies.⁽²⁵³⁾ Similarly, no corpora lutea form spontaneously in females in which pregnancy is maintained by exogenous progesterone (Anouassi and Tibary, unpublished; cf. Embryo transfer). Thus, the presence of 2 or 3 corpora lutea is likely to be due to multiple ovulations at the time of breeding (Table 11).
 

The incidence of multiple corpora lutea surpasses by far the incidence of twin (0.13-0.4%) or triple (0.13%) pregnancies in the dromedary (Table 12).^{(180, 212, 214)} In addition, all of the multiple pregnancies are found in the first trimester of gestation.^{(31, 179, 180)} This discrepancy between number of corpora lutea and number of fetuses can be explained by failure of fertilization of one ovum or an early reduction of twin pregnancies in the camel. Our embryo collection results, as well as abattoir and clinical observations, support both possibilities. The average number of embryos obtained from donors with two mature follicles at breeding was 1.7 whereas an incidence of twin pregnancies of only 0.4% is obtained in our herd. Although twin delivery has been reported in the dromedary, it is a very rare phenomenon. Of 840 pregnancy records in our practice, the number of females with double ovulation, twin pregnancies (diagnosed by ultrasonography), twin abortion, and birth of twins were respectively 151, 3, 1, and 0 records. The majority of twin pregnancies resulted either in a reduction to a simple pregnancy or loss of both conceptions.

In the Bactrian camel, the corpus luteum of pregnancy measures 26 mm on the average but can vary from 18 to 35 mm.^{(71, 72)}

In the llama, the weight and size of the corpus luteum are highly correlated with plasma concentration of progesterone until day 30 of pregnancy.⁽¹²⁾ The corpus luteum of pregnancy is generally larger than a day-9 corpus luteum but continues to grow and reaches its maximum size (16.3 ± 0.3 mm) at 21 days.^{(12, 46)} Ultrasonographic studies have shown that 14% of the corpora lutea of pregnancy in this species show a central cavity.⁽¹²⁾

In the alpaca, the diameter of the corpus luteum of pregnancy varies between 12 and 19 mm.⁽⁶⁰⁾ No further significant increase in weight or progesterone levels of corpora lutea above the values reached on day 8 were observed in pregnant females. Once the maximum development is reached (by day 8) the embryo prolongs the functional life of the corpus luteum without markedly affecting its size, total mass, or its rate of secretion. However, there is a significant decline in total progesterone content of luteal tissue on day 13, suggesting that this stage may represent the critical period for zygote survival.⁽¹¹¹⁾ A high incidence of double corpora lutea on the same ovary has been reported for alpacas ⁽⁶⁰⁾ but no secondary corpora lutea have formed following a single ovulation.⁽¹²⁾
 

Endocrine role of the placenta

The main endocrinological function of the placenta in camelidae is the production of estrogen. Production of estrogen by the conceptus has been determined in the dromedary as early as 10 days post ovulation.⁽²²⁵⁾ Higher estrogen production is observed in advanced pregnancy in the dromedary^{(15,17, 94, 95, 228)} and in the llama.^{(56, 149)} There is no strong evidence that the placenta of camelidae is involved in the production of a chorionic hormone ⁽⁴⁾ (Sghiri and Combamous, personal communication).

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