Journal of Agricultural and Veterinary Sciences, Qassim University, Vol. 2, No. 2, pp.

59-66 (January 2010/Muharram1431H)

59




Causes of Infertility in Female Camels (Camelus dromedarius)
in Middle of Saudi Arabia

A. Ali, F.A. Al-sobayil, M. Tharwat, A. Al-Hawas, and A.F. Ahmed
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, and Qassim University,
51452 Buraydah, Qassim, Saudi Arabia

(Received 3/11/2008; accepted for publication 4/5/2009)

Abstract. The objective of this study was to investigate the common infertility forms in female camels (camelus dromedarius) in the Central
Region of Saudi Arabia. Over two breeding seasons, a total of 447 female camels were examined for reproductive disorders. Based on
history, animals were categorized as repeat breeder (RB syndrome, n=343), refused mating (RM syndrome, n=73) and early embryonic death
(EED syndrome, n=31). Animals were then exposed to rectal examination, vaginal exploration and rectal ultrasonography. Results showed
that endometritis and metritis were the major causes of infertility (57.1%). Vaginal adhesions were the second important infertility problem
(16.1%) and recorded frequently in multipara than in nullipara animals (P<0.01). Ovarian cysts (5.3%) and ovarian inactivity (3.6%) did not
represent major infertility problems. Miscellaneous causes of infertility included anomalies of the genital tract (1.1%), hydrosalpinx (0.5%),
and vaginal tumors (0.5%).

Keywords: infertility; female camels; endometritis; vaginal adhesions, ovarian cysts.

A. Ali, et al.
60
Introduction
Reproductive efficiency in Camelidae is considered low (Tibary et al., 2005; Kaufmann, 2005). Calving
rates rarely exceed 40% in travelling herds and 70% in more intensively managed herds (Tibary and Anouassi,
1997). Thus, identification of reproductive diseases is important, especially when dealing with genetically
superior animals. There are limited studies describing the forms and incidence of reproductive disorders in
Camelidae, especially those linking clinical manifestations with the actual causes of infertility.
Generally, repeat breeding, refuse mating, and difficulties in the mating process have been reported as
common owner's complaints in female camels. Uterine infections, ovulation failure, and management errors have
been suggested as the actual causes of camel infertility (Wernery and Kumar, 1994; Tibary et al., 2001).
The major contributing factors to uterine infections in female camels are over breeding, postpartum
complications and unsanitary gynecological manipulation (Tibary et al., 2006). Ovulation failure is caused by
inadequate LH release in response to copulation (Skidmore and Adams, 2000). Aggressive mating during the
wrong phase of follicular developmental phase has been reported as a cause of severe uterine inflammation
(Tibary et al., 2001; Vaughan and Tibary, 2006). Other management errors include breeding with a young male,
overuse of males, and lack of verification of intromission during copulation (Tibary and Anoussi, 2000).
During the last decade, camels population in Saudi Arabia decreased from 426,015 in 1997 to 260,000
camels in 2007 (FAO, 2009). Investigation of the causes of this drop is important. Disturbances in reproductive
efficiency might be a factor in the progressive decline in the number of camel population in this country. The
aim of the present study was to describe the most common forms and incidence rates of reproductive disorders in
dromedary camels in the Central Region of Saudi Arabia, linking the regular owners complaints with the
clinical findings. The effect of parity on the incidence of these forms was also investigated.

Material and Methods
Animals
A total of 447 female camels (Camelus dromedarius) aged between 4 to 15 years were examined at the
Teaching Veterinary Hospital of Qassim University, Saudi Arabia for reproductive disorders. The study was
carried out during two breeding seasons (from September to March 2007-08). Of the examined animals, 152
(34%) were nulliparous and 295 (66%) were multiparous. All presented animals were already prophylactically
administered against trypanosomiasis using Quinapyramine sulphate and Quinapyramine chloride (Triquin

,
Wockhardt, Bumbai-India).
Breeding history (interval since last calving, number of times bred, milking status, male fertility, and
herd fertility) were recorded. The reproductive tract of each animal was examined by palpation per rectum and
exploration per vagina. Ovaries were carefully examined for structures and size. The uterus was palpated for
consistency, contractility, contents, and thickness. Vagina and cervix were examined for patency and discharges.
Transrectal ultrasound (Dynamic imaging LTD, Scotland-UK) attached with linear-array 7.5 MHz
transducer was used in cases where transrectal palpation was insufficient to reach a definite diagnosis, like those
suggested to have ovarian cysts, pyometra, hydrometra, or embryonic death. Clinical findings of each case were
recorded.

Criteria for classification of different syndromes
Individual animals were classified as one of the following groups:
Repeat breeder (RB syndrome).
animals that show estrus at regular intervals (12-14 days) but fail to conceive after 3 or more services.
Refuse mating (RM syndrome).
a female camel that curls her tail dorsally when approached by a rutting male.
Early embryonic death (EED syndrome).
animals which refuse the male 2 weeks after mating as if they were pregnant; however, later on (>30
days) they return to estrus and accept the male.
Endometritis / Metritis.
the uterus and / or cervix are enlarged, tough, and have thick wall, with different degrees of vaginal
discharges. According to the thickness of the uterine wall and the amount and consistency of the vaginal
discharges, endometritis / metritis were classified into three degrees (mild degree: uterus of normal consistency
with small amount of mucopurulant vaginal discharge; moderate degree: thick-walled uterus with moderate
Causes of Infertility in Female Camels

61

mucopurulant discharge; and severe degree: large-sized uterus with hard consistency and thick or pasty vaginal
discharges).
Ovarian inactivity.
both ovaries are small, smooth, firm, with no palpable follicles or corpus luteum, and the uterus is small
and atonic.
Ovarian cyst.
This was indicated by detection of a follicle exceeding 25 mm in diameter. Follicle theca cyst was
considered when the wall was thin and fluctuated, while the contents were homogenous and hypoechogenic. On
the other hand, follicle lutein cyst / or hemorrhagic cyst: was indicated when the wall was thick and hard,
while the contents were non-homogenous and echogenic (Tibary and Anouassi, 2000).

Histopathological examination
Tissue specimens were obtained from tumor-like structures on the vaginal wall and fixed in 10% neutral
buffered formolsaline, embedded in paraffin wax, sectioned at 5 microns and stained with haematoxylin and
eosin for histopathological examinations.
Statistical analysis
SPSS program (version 16, 2007) was used for data analysis. Significance level was put at P<0.05.

Results
All females included in this study (n=447) were non-lactating. In the case of multiparous animals a
period of 8 to 24 months (average 16.40.1 months) has elapsed since the last calving. Conception rate (animals
conceived / animals mated) in herds where these females originated ranged from 70.6% to 84.6% (average
74.9%, n=72 herds). The average number of services per conception in these herds was 1.81.0. All breeding
males in these herds were fertile based on the pregnancy rate of the mated females. All examined female camels
appeared clinically healthy.

The presented female camels were examined for RB (343/447, 76.8%), RM (73/447, 16.3%), and EED
syndromes (31/447, 6.9%). The number of previous services for the RB females ranged from 3 to 8 services
(average 5.40.6 services). Refuse mating lasted for a period of 50 to 140 days (average 947.4 days). Females
with EED syndrome returned for mating after a period of 30 to 90 days (average 46.76.7 days).

Clinical findings in different forms of reproductive disorders are shown in (Table 1). Collectively,
endometritis and vaginal adhesions were the main clinical findings in dromedary camels with reproductive
disorders.

Table (1). Frequency of different clinical findings in various syndromes in female camels examined for reproductive disorders
(n=447).
Clinical findings Frequency of Different Clinical Findings in
Various Syndromes n(%)
RB syndrome RM syndrome EED syndrome Total
Endometritis / Metritis 222 (64.7) 18 (24.7) 15 (48.4) 255 (57.1)
Vaginal adhesions 47 (13.7) 19 (26.0) 6 (19.3) 72 (16.1)
Apparently normal genitalia 49 (14.3) 6 (8.2) 10 (32.3) 65 (14.5)
Ovarian cysts 16 (4.7) 8 (11.0) 0.0 (0.0) 24 (5.3)
Ovarian inactivity 0.0 (0.0) 16 (21.9) 0.0 (0.0) 16 (3.6)
Pregnancy 0.0 (0.0) 6 (8.2) 0.0 (0.0) 6 (1.3)
Anomalies of the genital tract 5 (1.4) 0.0 (0.0) 0.0 (0.0) 5 (1.1)
Hydrosalpinx 2 (0.6) 0.0 (0.0) 0.0 (0.0) 2 (0.5)
Vaginal tumor 2 (0.6) 0.0 (0.0) 0.0 (0.0) 2 (0.5)
Total 343 73 31 447
RB: repeat breeding; RM: refuse mating; EED: early embryonic death

Endometritis / metritis were found in mild, moderate, and severe degrees in frequencies of 117/255
(45.9%), 77/255 (30.2%), and 61/255 (23.9%), respectively (Fig 1). Vaginal discharges were observed after
exploration of the vagina, but rarely during transrectal palpation. Chronic metritis accompanied with adhesions
A. Ali, et al.
62
of the uterus (not freely movable) to the broad ligaments, rumen, or omentum was recorded in 15/255 (5.9%) of
the cases. Parity did not influence the incidence of endometritis / metritis (90/152, 59.2% in nullipara vs.
165/295, 55.9% in multipara).
Vaginal adhesions completely closed the passage to the cranial part of the genital tract (Fig 2a). It was
associated with accumulation of hypo- or hyper-echogenic materials in the uterus in 26/72 (36.1%) of the cases (Fig
2a,b). The uterus was not distended in the other cases (46/72, 63.9%). The vaginal adhesions were found at caudal-,
mid-, or cranial -vagina in frequency of 13/72 (18.1%), 54/72 (75.0%), and 5/72 (6.9%), respectively. Some of the
examined cases (4/72, 5.6%) were presented with bleeding from mating, with a history of an incomplete
intromission of the penis. The adhesions were found as thick- or thin-walled in frequency of 52/72 (72.2%) and
20/72 (28.8%), respectively. Vaginal adhesions were observed more frequently (P=0.001) in multipara (61/295,
20.7%) than in nullipara (11/152, 7.2%), most of the multipara were over 10 years (43/61, 70.5%).
Ovarian cysts and ovarian inactivity did not represent major problems in examined female camels.
Follicle lutein or hemorrhagic cysts (17/24, 70.8%) were noticed more than the follicle theca cyst (7/24, 29.2%),
(P=0.01), (Fig 3). The frequency of ovarian cysts (7/152, 3.3% vs. 19/295, 7.3%) and ovarian inactivity (3/152,
2.0% vs. 13/295, 4.4%) did not differ significantly between nulli- and multi-para camels, respectively.
Vaginal tumors were observed in two cases of the RB syndrome. In the first case, the female-camel bled
just after mating and during vaginal manipulation (Fig 4a). Vaginal exploration revealed the presence of many
variable-sized round structures mixed with clotted blood and attached to the vaginal wall (Fig 4b).
Histopathologically, the case was diagnosed as an adenocarcinoma (Fig 4c). In the other case, a single large-
sized soft structure was palpated on the lateral side of the vaginal wall, about 10 cm cranial to the lips of the
vulva (Fig 5). Histpathological examination verified the tumor as a lipoma.
Anomalies of the genital tract were recorded in five cases. Partial or complete closure of the lips of the
vulva were observed in 2 cases (Fig 6a,b), one of the cases was accompanied with narrowing of the vagina. Two
cases were observed with enlargement of the clitoris, but the rest of the genital tract was normal (Fig 6c).
Imperforated hymen with accumulation of a viscous milky material in the anterior vagina was observed in one
case (Fig 7a,b). This animal was presented with a history of difficult mating process. Unilateral hydrosalpinx
was observed in two cases of RB syndrome. The fallopian tube was palpated per rectum as a distended fluctuated
tortuous structure. Ultrasonographic examination revealed many hypoechogenic well demarcated sacs adjacent
to the ovary (Fig 7c).

Discussion
The Results demonstrated that the herd fertility in the Central Region of Saudi Arabia lies between 71
and 85%, which is slightly lower than that reported by Arthur et al. (1996) in the Eastern Region of the Kingdom
(80 to 90%). Yagil (l985) reported similar findings. His experimental dromedaries attained a fertility rate of
100%. However, when kept under conditions of intensive husbandry, Mukasa-Mugerwa (1981) reported a
dromedary fertility rate of only 50%, which could be improved up to 65% with corresponding improvements in
management.
The current study revealed that endometritis / metritis were the major components of infertility in
dromedary camels raised in the Central Region of Saudi Arabia. Overbreeding has been suggested as a major
contributing factor to uterine infection (Tibary et al., 2001; Tibary, 2004a). In Camelidae, during mating, the
penis penetrates the cervical canal and enters deep into the uterine cavity (Vaughan and Tibary, 2006). Repeated
insults of the uterus due to improper mating practices can lead to inflammation and loss of the ability to resist
infection (Tibary et al., 2006). Moreover, as camelidae are induced ovulators, aggressive mating during the
wrong follicular developmental phase can induce severe uterine inflammation (Tibary et al., 2001; Vaughan
and Tibary, 2006). Resistance of the uterus to infection and its ability to rid itself of microorganisms was also
diminished in the presence of degenerative changes in the endometrium or repeated heavy infection with
pathogenic strains (Tibary 2004a,b). Results of the current study indicated that the incidence rates of
endometritis in nullipara were similar to those observed in multipara. This result may support the opinion that
wrong mating might be the primary cause of endometritis. Other contributing factors to endometritis were
postpartum complications and unsanitary gynecological manipulation (Tibary et al., 2001; Tibary, 2004b).
Clinically most female-camels with endometritis / metritis showed behavior of repeat breeding, but others
refused mating, or returned for mating after variable periods of anestrous.
Vaginal adhesions were the second important infertility problem in dromedary camels; nevertheless this
study suggests that the problem is the most threatening one for the reproductive life of the affected animals, as
Causes of Infertility in Female Camels

63

most of them were discarded from breeding due to occlusion of the genital tract. The pathogenesis of the
problem was not clear, as most of the examined animals were purchased with no reproductive history. Chronic
vaginitis, overbreeding, aggressive mating practice, injuries during parturition, increasing parity could be
suggested as factors which contribute to the problem. Moreover, some herdsmen place unusual substances, like
dates, black seeds, and salts in the vagina of animals with fertility problems as a part of ethoveterinary practice.
These substances may be irritant to the mucus membrane of the vagina predisposing or leading to the problem.
Based on the duration of the condition, the uterus was found either apparently normal, or filled with viscous or
even purulent materials. Refuse mating for long time, difficulties in the mating process, or bleeding just after
mating are typical clinical signs of the vaginal adhesion in dromedary camels. The condition of vaginal
adhesions has been reported in the literature (Tibary et al., 2006), however the authors did not document the
incidence or the seriousness of the problem. In this concern, veterinarians should differentiate between the cases
of vaginal adhesions and those with persistent hymen. The latter is a congenital condition that is found only in
nullipara, usually located just cranial to the external opening of the urinary bladder, and has good prognosis. In
contrast, vaginal adhesions are an acquired process that is observed mostly in aged multiparous animals, locates
mainly in mid- or cranial vagina, bleeds easily at manipulation, and has bad prognosis on fertility. However, in
nulliparous females, we have not attempted to differentiate between vaginal adhesions and congenital vaginal
aplasia or segmental aplasia.
The genital tract was found apparently normal in a proportion of female-camels presented with different
forms of reproductive disorders. Subclinical endometritis, hormonal disturbances, male factors, or errors in
management might be the reasons for this phenomenon (Tibary and Anouassi, 1997). Different types of
pathogenic bacteria were isolated from the genital tract of that category of females (Ali et al., unpublished data).
Ovarian cysts did not constitute a major infertility problem in the investigated female camels. Although
ovarian cysts have been described in dromedaries (Shalash and Nawito, 1963; El-Wishy, 1990; El-Khouly et al.,
1990), the cystic ovary condition is not well documented as in cattle or other domestic animals. In fact, the term
"cystic ovaries" does not always apply to Camelidae because some females develop follicular cyst if not bred, as
ovulation in these species is induced (Tibary et al., 2005). Moreover, ovulation failure after adequate mating
might be a cause of repeat breeding in Camelidae. Ovulation rate in a well managed herd ranges from 80 to 90%
(Tibary and Anouassi, 1997; Tibary et al., 2005). Ovulation failure might be caused by inadequate LH release in
response to copulation (Tibary and Anouassi, 1997; Kaufmann, 2005). In this study, repeat breeding and refuse
mating were the clinical symptoms of females with ovarian cysts.
Similarly, ovarian inactivity did not constitute a large proportion of female camel infertility. The reason
for that might be the optimum breeding season in which the current study was carried out and during which most
animals were cyclic. Actually, this problem is not fully investigated in Camelidae as in other domestic animals.
Miscellaneous causes of female camels infertility included anomalies of the genital tract, hydrosalpinx,
and vaginal tumors. Some of these problems have been recorded in previous studies (El-Wishy, 1990, Ramadan,
1997; Mesbah et al., 2002), however, most of these problems have been recorded only in the slaughterhouses,
and their effects on fertility have not yet been described.
In conclusion, endometritis / metritis are the most common forms of infertility in dromedary camels
raised in the Central Region of Saudi Arabia. Vaginal adhesions constitute a serious infertility problem, because
it has bad prognosis on the reproductive life of affected females.

Acknowledgements: This study was supported by the Deanship for Scientific Research, Qassim University
Saudi Arabia.
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64
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