Diseases of the Ovaries and Ovarian Bursa

Many ovarian and bursal pathologies described in other domestic species have also been found in the camelidae and include inflammatory and degenerative processes. Studies on thousands of genital tracts from slaughtered animals show an incidence of ovario-bursal pathology ranging from 1 to 21%.^{(3, 9, 10, 29, 44, 45, 47-49, 94, 95, 99, 103)} However, there are no clinical studies on the effect of these pathologies on infertility in this species. Data from our laboratory shows that ovarian pathology, and particularly ovario-bursal adhesions, is responsible for a great number of long-standing infertility cases in the dromedary. ⁽¹¹⁸⁾

In llamas and alpacas, ovarian pathology reported in animals with histories of infertility following repeated breeding include hypoplastic ovaries (no follicular growth or growth limited to 6 mm), ovulatory failure, and cystic follicles.^{(4, 29, 58, 109, 110)}

Cystic conditions of the ovary

Cystic conditions of the ovaries are of two types: cysts within the ovary itself (ovarian cysts) such as follicular or luteal cysts, and cysts outside of the ovarian tissue usually called paraovarian cysts. Although types of ovarian cysts have been described in the llama,⁽²⁹⁾ alpaca,⁽²⁹⁾ dromedary, ^{(3, 44, 46-48, 86, 99, 103, 104)} and Bactrian camel,⁽³⁴⁾
cystic ovary conditions are not as well defined as those described in cattle or other domestic animals. Given the fact that ovulation in these species is induced, the term 'cystic ovaries' does not always apply for camelidae because a large proportion (30 to 40%) of females develop some form of follicular cyst if not bred (cf. Physiology).⁽¹¹⁷⁾

Paraovarian cysts

Paraovarian cysts are fluid-filled structures located in the broad ligament near the ovary or uterine tube. They could be just remnants of the mesonephric (Wolfian) or paramesonephric (Mullerian) duct system. They can be single or multiple, unilateral or bilateral, round or oval, measuring 0.5 to 5 cm in diameter (Figure 8.1).

Their effect on fertility is not known. We have found several of these cysts in animals at different ages and with different reproductive history. They are sometimes just an incidental finding during ultrasonography but should be differentiated from distention of the uterine tube with fluid (hydrosalpinx) or collection of fluid within the bursa. Their real incidence is not known. Para- or peri-ovarian cysts tend to grow very slowly or remain at the same size.

Ovarian cysts

Ovarian cysts are described according to the structure involved and their appearance as follicular cysts, luteal cysts, cystic corpora lutea, and hemorrhagic cysts according to their histological and physical characteristics (Figure 8.2). All these types of cysts have been described in llamas, alpacas and dromedaries (Table 3). Only follicular cysts have been described in the Bactrian camels and are associated with infertility.⁽³⁴⁾

Our observations in more than 5000 ultrasonographic examinations in the dromedary suggest that follicular and hemorrhagic cysts are a normal evolution of the non-ovulatory follicle in 30 to 40% of the females.^{(15, 117)} Similar observations have been made in the llama.⁽⁵⁾ This is why there is a great difference in the incidence of ovarian cysts found by different authors. Incidence is very low to nil in bred females ^{(3, 10, 16, 18, 20, 78)} and can reach 30 to 40% in non-bred females.^{(5, 15, 106, 107, 117)} Some authors have found an increased incidence of from 4% to 8% in infertile alpacas which suggests that part of these cysts reflect some pathology in the ovary (probably insufficient LH release and consequently ovulation failure).⁽¹¹⁰⁾ Incidence of follicular cysts or anovulatory follicles is increased in some females following superovulatory treatment with FSH or eCG (PMSG).⁽⁷⁵⁾ This is probably caused by insufficient LH release to induce ovulation of all follicles in superovulated females following mating. In our experience, anovulatory follicles do no have any negative effect on a newly emerging follicular wave and ovulation of a new follicle is possible even in the presence of these structures. However, some of these anovulatory follicles can become luteinized, producing enough progesterone to induce decrease in uterine tone and rejection of the male. Luteinized cysts can also be the result of partial luteinization of a follicle following breeding.
 

Cystic corpora lutea represent a normal morphology in a proportion to corpora lutea and do not seem to effect their function. Cystic corpora lutea have been found regularly in pregnant animals without effect on pregnancy. These cystic CL usually have a larger diameter and their luteinization progresses slowly toward complete luteinization with advancing stages of pregnancy.

Diagnosis

Cystic conditions of the ovaries are easily diagnosed by rectal palpation and ultrasonography. They are large, spherical structures projecting from the ovary and can be single or multiple. In the llama and alpaca they can reach up to 5 cm in diameter and in the dromedary they can be as large as 12 cm in diameter and can weigh as much as 250 g.^{(48, 117)}

Follicular cysts are thin-walled and grayish-brown. Solitary follicular cysts predominate but bilateral cysts are not rare. Histologically, the cysts are lined by flattened-cuboidal epithelial cells. There are 1 to 5 rows of granulosa cells with fibroblastic proliferation on the outside of the epithelial layer.⁽¹⁰⁾ The content of the cyst is light-yellow to reddish-brown.⁽⁴⁸⁾

Hemorrhagic cysts have a thicker wall than follicular cysts and have a peculiar echotexture resembling a hematoma. The content can be red fresh blood or a blood clot surrounded by serum.

Luteal cysts are usually single, thick-walled, grayish-yellow, and smaller in size than follicular cysts. They are filled with grayish-brown fluid and originate from luteinization of follicular cysts. The cyst wall is lined by polyhedral-spherical cells with vacuolated cytoplasm (lipid-containing cells) and pyknotic nuclei.⁽¹⁰⁾ These luteal cysts are relatively easy to identify by ultrasonography.

Although the role of ovarian cysts in causing infertility in camels is not known, an incidence of 4.7% was reported in a random sample of slaughtered alpacas while a higher frequency of 8.3% was reported in specimens collected from infertile animals.⁽¹¹⁰⁾ However, in a study on llamas, failure to become pregnant was not associated with the formation of a hemorrhagic follicle.⁽⁵⁾ In Bactrian camels, cystic follicles were detected on the ovaries of a female inseminated unsuccessfully with semen from a fertile male in two successive seasons.⁽³⁵⁾

There are very few studies dealing with the endocrinology of cystic conditions of the ovaries. In one study on llamas and alpacas, animals with cystic follicles showed a decrease in estrogen secretion with the appearance of the cystic follicle (follicle became larger than 12 mm).⁽²⁹⁾ In many females, these cysts become luteinized under the influence of LH released in response to copulation or even spontaneously. The effect of cysts on ovarian activity is variable. In early stages of the condition, the cysts seem to inhibit follicular development beyond 6 mm size. However, normal follicular development and ovulation is also possible in some females. This variation of the effect of cysts on follicular activity may be dependent on the nature of the cyst and its endocrine activity.⁽²⁹⁾ Similar observations were made by our group in the dromedary female. Plasma progesterone assays in our laboratory showed that these so-called cysts can become luteinized and secrete enough progesterone to simulate the presence of a functional corpus luteum. Analysis of our examination records show that anovulatory follicles tend to appear in the same females every year. Also, it is important to note that this luteinization, which concerns about 33% of anovulatory follicles, can occur even in the absence of mating. When females presenting anovulatory follicles (> 35 mm in diameter) are treated with 4500 to 5000 IU of hCG. luteinization occurs in 45% of the cases as detected by ultrasonography and a plasma progesterone level > 2 ng/ml (Tibary and Anouassi, unpublished). Estrogen and progesterone content in the cystic fluid of two specimens revealed levels of 406.6 and 458.1 pg/ml, and 47.8 and 65.0 ng/ml respectively.⁽⁴⁸⁾

Treatment

The overwhelming majority of the "follicular cysts" in the female camelidae do not warrant treatment. This is because they are a normal outcome of the mature follicle in the absence of breeding in 40 to 50% of the females and do not seriously affect follicular activity. The incidence of these anovulatory follicles is greatly reduced if the females are in a breeding group. Many practitioners attempt to manually rupture the anovulatory follicles. This practice should be discouraged because of the risk of bleeding in the bursa and development of ovario-bursal adhesions. Some luteinized anovulatory follicles respond to a luteolytic dose of PGF2α or its analogue. Therefore, in the dromedary, a therapeutic approach to this condition is to first induce luteinization with 5000 to 10.000 IU of hCG (human Chorionic Gonadotropin) followed 5 to 6 days later by an injection of PGF2α or its analogue. Injection of PGF2α or its analogue may need to be repeated at 24 hours. Elimination of anovulatory follicles is sought mainly in donors because the presence of these structures can physically compromise superovulation. This can be achieved by daily injection of progesterone (100 mg per animal) for 10 to 15 days.⁽⁷⁴⁾ Females that have the tendency to develop anovulatory follicles because of failure of ovulation should be given hCG one hour after breeding.

Ovarian inactivity

Absence of ovarian follicular activity is a frequent condition in camelidae. Although many authors have reported that the female camelidae is seasonal with a physiological period of ovarian inactivity, this holds true only under harsh management conditions. Seasonality in the female camelidae has been described in detail elsewhere in this publication (cf. Physiology of reproduction in the female). In fact, most of the camelidae will have ovarian activity all year round if they are in a very good nutritional state. In many species, lack of ovarian activity will induce a state of prolonged anestrus. The term "anestrus" cannot be used in the female camelidae because of a highly variable behavior towards the male which is not very well correlated with follicular activity. Absence of follicular activity can be due to congenital or acquired ovarian hypoplasia.

Incidence and etiology

The incidence of ovarian hypoplasia in the dromedary varies from 0.2 to 6%.^{(10, 47, 48, 99, 103, 104)} In our laboratory, ovarian inactivity was found to be greatly affected by the body condition and use of the animal (Table 4).
 

Ovarian inactivity is very common in females just retired from racing and in females with a low body condition score (< 3, cf. Management of reproduction). Hypogonadism and ovarian hypoplasia are therefore due mainly to inadequate nutrition. There are no reports on ovarian hypoplasia due to genital or chromosomal abnormalities in camelidae but this possibility should not be discarded.

Diagnosis

Clinical diagnosis of ovarian inactivity or hypogonadism is based on rectal palpation and ultrasonography. The ovaries are very small and hard with a smooth surfaced.⁽⁴⁸⁾ The ovarian size is usually half to a third of the normal size.^{(29, 48)} In some cases, the ovaries are so small and devoid of follicular activity that their palpation or visualization with ultrasonography becomes nearly impossible. Monitoring of ovarian activity by ultrasonography is very important in order to confirm this problem. In the dromedary camel we expect to see some follicular development with at least one complete follicular wave leading to the development of a mature follicle within a 15-day period. Ovarian inactivity or hypogonadism is suspected if no activity or only limited follicular development is observed during this period. Follicular development may be seen in some females, but the number of follicles recruited is limited to one or two and these follicles fail to develop to an ovulatory size.⁽²⁹⁾

Endocrinological abnormalities, especially hypothalamic and pituitary inactivity, may be involved in the onset of ovarian inactivity but no data is available on the profile of LH and FSH in hypogonadic females. Nearly all the cases that we observe in the dromedary are due to a poor body condition or chronic health problems. Acquired ovarian inactivity should be differentiated from lack of, or reduced, activity in prepuberal animals.

Treatment

Adequate treatment of ovarian inactivity relies on the determination of the underlying causes. In our experience, poor body condition or debilitating diseases are the main cause of acquired hypogonadism. Many authors have suggested administration of gonadotropin (eCG or FSH) for the treatment of this condition.⁽³⁸⁾ Although these treatments can stimulate follicular development and eventually ovulation after breeding, the pregnancy rates remain poor because of increased incidence of abnormal corpora lutea and early embryo death. In addition, follicular response to these hormones is very variable and can lead to the development of many follicles and eventually fertilization of several ova which increases the risk of early embryo loss. A more logical approach is to first remedy the underlying cause by providing adequate nutrition and care. In our case, the number of females with inactive ovaries is greatly reduced by using a nutritional "flushing" about one month before the beginning of breeding.

Persistent corpus luteum

Persistent corpora lutea are very rare in the female camelidae. However, the condition has been suspected in llamas on the basis of prolonged high plasma progesterone level.^{(4, 103)} In our experience, and based on ultrasonographic monitoring of 680 animals in our embryo transfer program, we have never diagnosed a persistent copora lutea per se in the dromedary. However, in some cases progesterone remained high (> 2 ng/ml) for 15 days or more in the absence of mating and corresponded to luteinized anovulatory follicles which tend to have a very slow regression. Persistent corpora lutea should be easy to treat by injection of a luteolytic dose of PGF2α or its analogues.    However, PGF2α has been increminated in the death of some llamas and may be very toxic in these species. No adverse reaction has been observed in our practice in dromedaries receiving up to twice the bovine dose of this drug (cf. Hormonal therapy, Artificial breeding).

Ovario-bursitis with encapsulation of the ovary

Ovario-bursitis is a particular affection of the ovarian bursa characterized by the accumulation of variable amounts of fluid and encapsulation of the ovary (hydrobursitis) (Figure 8.3).⁽¹¹⁸⁾ This affection has been reported only in the dromedary camel.
 

Incidence

Ovario-bursal adhesions have been reported with varying frequencies in the dromedary (0.5%, ⁽⁷⁸⁾ 2.2%, ⁽⁹⁹⁾ 13.9%,⁽⁴⁴⁾ and 15.2% ⁽⁸⁶⁾).

A retrospective study on all cases diagnosed in our clinic shows that the overall incidence of hydrobursitis is 9.3% of all examined animals.⁽¹¹⁸⁾ The incidence of this pathology is relatively higher in animals with a history of reproductive failure and was 37.5%, 35.1%, and 21.4% higher, respectively, for females that had aborted, were barren more than 2 years, or were infertile for 1 to 2 years. The lowest incidence was found in females that had recently calved (0.1%). These results indicate clearly that this pathology is a cause of infertility or reproductive wastage in adult females, and can occur any time during the life of the individual as demonstrated by a 3.5% incidence in maiden females. The presence of pregnancy in many unilaterally affected females suggests that the non-affected side continues to function normally. However, there was an increased incidence of abortion and embryonic death in the affected pregnant females. In one study, the affection was bilateral in 62.3% and unilateral in 37.7% of the cases.⁽⁴⁴⁾ However, in our case, the incidence of bilateral cases was about one third that of unilateral cases. Both left and right sides were affected, with an incidence in the left side twice that of the right side. Bilateral affection was more frequent in females with long-standing infertility (more than 2 years). None of the females affected by the condition showed any other sign of illness.⁽¹¹⁸⁾

Ovario-bursitis has been reported in two other studies, with an incidence of 13.9% in the United Arab Emirates⁽⁴⁴⁾ and 15.2% in Somalia.⁽⁸⁶⁾ Salpingitis and ovario-bursal adhesions were not seen in any of hundreds of specimens examined by other authors in Egypt⁽⁴⁹⁾ and Saudi Arabia⁽¹⁸⁾ and only one case (associated to hydrosalpinx) was reported after examination of 216 specimens in Sudan.⁽⁷⁷⁾ These latter authors suggested that the rarity of this condition can be ascribed to either the scarcity of uterine infections or the peculiar anatomy of the utero-tubal junctions in the camel. We disagree with this view because uterine infection in the dromedary is as prevalent as in other species. The association between hydrobursitis and other disease processes remains to be studied. In one study, 40% of the hydrobursitis cases were associated with echinococcus infestation, but the significance of this association remains unclear.⁽¹⁰³⁾

Diagnosis

Diagnosis of hydrobursitis is done with rectal palpation and ultrasonography. The condition is suspected when difficulty is encountered during retraction of the uterus or when reaching for and grasping the ovaries is attempted. In some cases, the oviduct presents a severe torsion, easily identified by palpation (cf. Surgery of the female reproductive tract). However, the pathology cannot be detected on the basis of palpation alone if the amount of fluid is small. Ultrasonography is a more reliable diagnostic technique when performed by an experienced veterinarian. The appearance of the ovarian-bursa and its content is variable and depends on the size, ovarian activity, and the nature of the fluid within the bursa. In the majority of cases, the fluid is anechoic (Figure 8.4). However, in a few cases the bursal content presents some echogenicity and sometimes a line of demarcation is seen corresponding to the settling of the cellular material at the bottom of the structure (Figure 8.4). The ovary most often appears floating inside the bursal sac and is easily identified when active. Ovarian activity within the bursal fluid ranges from inactivity to the presence of follicles, large cyst-like structures, or corpora lutea. In a few cases, various amounts of adhesion can be identified as strands of floating material within the bursa (Figure 8.4).
 

Pathology

The characteristics of the lesions obtained at the slaughterhouse or after surgery are summarized in Table 5. The color of the content ranges from a clear amber color resembling that of follicular fluid to a dark hemorrhagic appearance. The content of the lesions can be categorized into 5 types according to the consistency and color of the fluid (Figure 8.5).

The size of the affected bursa ranges from 15x15 cm to a maximum of 42 x 25 cm and the content from a few milliliters to 10 litres. The consistency of the bursal content varies from watery to highly viscous - almost gelatinous. In some cases, floating proteinaceous concretions are encountered upon dissection of the bursal cavity (Figure 8.5). Although most (83%) of the cases present a unique cavity with the ovary encapsulated within it, a few (17%) are found with the ovary encapsulated in a separate cavity within the larger one, or completely outside of the lesion (Figure 8.5). In some cases, adhesions can be seen within the bursal cavity. Ovarian activity, mainly follicular (follicles or cyst-like formations), can be seen in encapsulated ovaries without adhesions. In females with follicular activity, ovulation and corpus luteum formation is possible after breeding or treatment with hCG or GnRH (Figure 8.4). In about one third of the cases seen in our clinic, the condition is associated with oophoritis or salpingitis or both. The oviduct is patent on the affected side in about half of the cases.⁽¹¹⁸⁾ Biochemical analysis of the bursal fluid suggests that it is probably a mixture of blood and follicular fluid.

Etiology

A retrospective study on all of the ovario-bursal pathologies cases treated in our clinic allowed us to consider some hypotheses concerning the etiology of hydrobursitis which are currently being investigated.⁽¹¹⁸⁾ These hypotheses are in order of likelihood as follows:

1)    A possible relationship between recurrent anovulatory hemorrhagic follicles and bursal adhesions. It is possible that encapsulation of the ovary and collection of fluid result as a complication from successive ruptures of hemorrhagic follicles and formation of ovario-bursal adhesions. We are pursuing this theory by studying the fate of the non-ovulating follicles in regular examinations of all the camels under our supervision. Our initial results show that in the absence of mating (lack of the ovulation-induction mechanism) the mature follicle kept on growing in 35% to 50% of the females and reached sizes as large as 12 cm in diameter. A fraction of these anovulatory follicles became hemorrhagic then ruptured or formed a well-organized structure similar to a blood clot or to a partially luteinized follicle. If these structures rupture within the bursa there is sufficient blood supply to induce a small hemorrhage which later can lead to the development of adhesions. In the llama, substantial hemorrhage can be observed after rupture of the anovulatory follicles because of the presence of anticoagulant substances.⁽⁵⁾

2)    Relationship between this pathology and other uterine oviductal pathology. Contrary to what was previously published, there is a high incidence of genital tract infection in the dromedary. In some cases the hydrobursitis is associated with salpingitis which could suggest the involvement of infection or an acute inflammatory process with occlusion of the oviduct. Although our bacteriological examinations of the fluid from cases of hydrobursitis were negative, other authors have isolated Actinobacillus sp, and E.coli from such cases.⁽¹²⁾ The condition can be also caused by chronic infection with compylobacter or brucella.⁽¹²⁴⁾

3)    Presence of a genetic predisposition. This hypothesis is included because of the fact that the camels that we are dealing with are all from the UAE and bred in a closed system for racing purposes. Also, the authors did not observe any similar cases in slaughtered camels in Morocco. This genetic predisposition could be linked to the fact that some females are more prone to develop anovulatory hemorrhagic follicles than others.
 

Type I:    Brown, thick muddy appearance with high cellular content
Type II: Hemorrhagic, dark red fluid with high cellular content
Type III: Serous, blood tinged, yellow-pink with low cellular content
Type IV: Serous clear to amber, almost watery. No cellular content
Type V: Very thick, white-yellowish, pus appearance, very high cellular content
 

Treatment

Treatment of hydrobursitis is to be considered in the case of valuable animals. The only available treatment of hydrobursitis cases is the surgical removal of the affected bursa and ovary. Surgical technique is described elsewhere in this publication (cf. Surgery of the female reproductive tract). This technique has been used on 21 unilaterally affected females with a 53% pregnancy rate following breeding 4 weeks after surgery. Unsuccessful surgery is mainly due to complications with peri-uterine adhesions, early embryonic death, or abortion.⁽¹¹⁸⁾

In bilaterally affected animals, ablation of both ovaries and ovarian bursa followed by embryo transfer has been attempted with some success in a few females.⁽¹¹⁸⁾ Although this technique does not save the reproductive ability of the female per se, it can be considered for production of milk from a particular female or as a means of preparation of a recipient in an embryo transfer program. Exogenous hormonal preparation and maintenance of pregnancy in these cases is necessary and is described in a later chapter (cf. Embryo transfer). A third treatment technique is being investigated in our laboratory and consists of excision of the ovarian bursa without removal of the ovary in order to save the reproductive ability of superior females. This approach would allow the use of the female as an oocyte donor in an in vitro fertilization program. Obviously such a procedure is only justifiable if there is no involvement of the ovary in the pathology and follicular activity is maintained.

Ovarian tumors

Ovarian tumors have been described in several animal species including camelidae. They are generally grouped into 3 different categories according to their origin and histological characteristics: primary epithelial tumors (papillary adenoma, papillary carcinoma, cystadenoma, cystadenosarcoma), tumors of the sexual cord and ovarian stroma (granulosa cell tumor, theca cell tumor, interstitial cell tumor, luteoma), tumors of germinal cells (teratomas, dysgerminoma) and mesenchymal tumors (hemangioma, leiomyoma, fibroma, lymphoma).^{(73, 119)} Our observations, as well as those of others, show that ovarian neoplasms do not constitute a major cause of reproductive problems in camelidae. The incidence of ovarian tumors in camelidae varies between 0.06 to 2% and most of these are teratomas.^{(45, 47, 48, 99)}

Ovarian teratomas are benign tumors that originate from the germ cells and usually affect only one ovary. They do not seem to have any effect on follicular activity of the contralateral ovary. They tend to grow very slowly and the affected ovary is usually just slightly increased in size, although tumors as heavy as 277 g have been reported in the dromedary.^{(44, 45)} The ovarian mass presents different types of tissues including cartilage, bone and hair (Figure 8.6). These tumors are detected on routine palpation and ultrasonography and present different consistency and ultrasonographic appearance according to the type of tissue present. The ovary may appear completely hyperechoic or heterogeneous with several anechoic pockets corresponding to cysts.

Dysgerminoma is another type of ovarian tumor of germ cell origin. It has been reported in the dromedary camel but is extremely rare.⁽⁴⁴⁾ The effect on the health of affected animals is not known but in other species they are malignant and can cause rapid deterioration of the animal's condition after metastasis to the thoracic and abdominal cavities.⁽¹¹⁹⁾

Inflammatory disorders of the ovaries

Inflammation of the ovaries (oophoritis or ovaritis) may be secondary to an ascending infection from the uterus via the uterine tube or by extension of a peritonitis or perimetritis. It is characterized by loss of follicular activity because of the presence of adhesions between the ovarian surface and the surrounding tissues including the ovarian bursa, uterine tube, and sometimes extending to include some intestinal loops (Figure 8.7). Diagnosis of this condition is based on palpation and ultrasonography. Depending on the extent of the adhesions, the ovary may be very difficult to identify or manipulate per rectum. Confirmation of the diagnosis can be done by exploratory laparotomy or endoscopy. No studies have been done on the exact etiology of ovarian inflammation but it can be stated that severe endometritis, especially during the postpartum period, can contribute greatly to the incidence of this pathology.    Also, specific infections such as tuberculosis, brucellosis, and campylobacteriosis may be involved in this aafection. Ovarian inflammation and adhesions can also result from hemorrhage due to harsh manipulation of the ovaries or attempts to rupture anovulatory hemorrhagic follicles. Chronic localized inflammation of the ovary accompanied by abscess formation near the ovary has been encountered in a few cases (Figure 8.7). In some cases both ovaries can be involved and attached to the intestines or surrounding tissue making palpation very difficult (Figure 8.7).
 

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