Accepted Manuscript
Title: Dystocia in dromedary camels: prevalence, forms, risksand hematobiochemical changes
Author: Ahmed Ali Derar Derar Mohamed Tharwat MoustafaM. Zeitoun Fahd A. Al-Sobyil
PII: S0378-4320(16)30220-2DOI: http://dx.doi.org/doi:10.1016/j.anireprosci.2016.05.004Reference: ANIREP 5418
To appear in: Animal Reproduction Science
Received date: 29-2-2016Revised date: 27-4-2016Accepted date: 4-5-2016
Please cite this article as: Ali, Ahmed, Derar, Derar, Tharwat, Mohamed,Zeitoun, Moustafa M., Al-Sobyil, Fahd A., Dystocia in dromedary camels:prevalence, forms, risks and hematobiochemical changes.AnimalReproduction Sciencehttp://dx.doi.org/10.1016/j.anireprosci.2016.05.004
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1
Revised Clean
Dystocia in dromedary camels: prevalence, forms, risks and
hematobiochemical changes
Ahmed Ali1,3, Derar Derar1,3, Mohamed Tharwat1,4, Moustafa M. Zeitoun2, Fahd A. Al-Sobyil1
1Department of Veterinary Medicine, 2Department of Animal production, College of Agriculture
and Veterinary Medicine, Qassim University,
51452 Qassim, Saudi Arabia
3Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, 71526
Assiut, Egypt
4Department of Animal Medicine, Faculty of Veterinary Medicine, Zagazig University, Egypt
Authors:
Ahmed Ali: Professor of Theriogenology; [email protected]
Derar Derar: Professor of Theriogenology; [email protected]
Mohamed Tharwat: Professor of Internal Medicine; [email protected]
Moustafa Zeiton: Professor of Animal Production; [email protected]
Fahd Al-Sobyil: Professor of Clinical Sciences; [email protected]
Place of work:
Veterinary Teaching Hospital, Department of Veterinary Medicine, Faculty of Agriculture and
Veterinary Medicine, Qassim University, Saudi Arabia.
Corresponding author:
Ahmed Ali, Saudi Arabia, Qassim University, Faculty of Agriculture and Veterinary Medicine,
Department of Veterinary Medicine, Qassim, Burayda, Mulaydaa, postal code 51452, box office
6502; E-mail: [email protected] and [email protected]
2
Highlights
Dystocia in camels was observed more frequently in intensive than in free systems.
Postural abnormalities and uterine torsion were the most common forms of dystocia.
Duration of dystocia has an important bearing on fetal and maternal outcomes.
Dystocia was associated with increases in the acute-phase proteins, AST and BUN.
Abstract
The objectives of this study were to investigate the prevalence of dystocia in camel herds, its
forms in primi- and multipara, the risks to fetus and dam, and the associated hematobiochemical
changes. A total of 1890 calvings were surveyed for the prevalence of dystocia. Cases with
dystocia (n = 107) were examined for causes and treated with traction, fetotomy or Cesarean
section. Logistic regression was performed to identify risk factors. The dependent variables were
the fetal and maternal mortality, while the independent variables were parity, duration of
dystocia, causes of dystocia, and method of treatment. Blood samples were collected from all
dystocia camels and six controls for hematology and concentrations of serum amyloid A (SAA),
haptoglobin (Hp), estradiol-17β (E2), progesterone (P4), total protein, albumin, calcium,
phosphorus, magnesium, blood urea nitrogen (BUN), creatinine and aspartate aminotransferase
(AST). The overall prevalence of dystocia was 8.6%. Risk of dystocia was higher in camels
managed in an intensive system than in those in a free system (Odds ratio = 1.9, P = 0.0003) and
higher in primipara than in multipara (Odds ratio 1.7, P = 0.005). Abnormal posture was the
most important cause of dystocia (51.4%). Uterine torsion was the second most important cause
(23.4%) and was mainly observed in multipara (P = 0.0006). Dystocia was linked to high fetal
mortality (87.9%). A significant relationship was found between fetal death and duration of
dystocia (Odds ratio = 8.04, P = 0.005). The percentage of dam mortality was 17.8%. Significant
associations were detected between dam mortality rate and the duration of dystocia (Odds ratio =
4.74, P = 0.03) and fetal viability (Odds ratio = 5.82, P = 0.02). Increasing duration of dystocia
was associated with significant increases in SAA, Hp, BUN and AST, but with decreases in E2
(P < 0.05). After a transient period of elevation, the white blood cell and neutrophil counts
decreased (P < 0.05). In conclusion, abnormal posture and uterine torsion were found to be the
3
common causes of dystocia in dromedary camels, and fetal and maternal deaths were mainly
associated with the duration of dystocia.
Keywords: camels; obstetrics; mortality; hemogram; blood chemistry.
1. Introduction
In livestock industries, dystocia is a main factor in reduced productivity, including fetal and
maternal losses, subsequent infertility, culling rate, and cost of treatment (Tenhagen et al., 2007;
Mee, 2008; Uematsu et al., 2013). The direct causes of dystocia differ from one species to the
other. In mares, dystocia is most often caused by an abnormal presentation, position, or posture
(Vandeplassche 1987; 1993; Noakes et al., 2009; McCue and Ferris, 2012). In cows, feto-pelvic
disproportion is common, especially in primipara (Nix et al., 1998; Noakes et al., 2009; Mee,
2012; Mee et al., 2012). In camels, little is known about the forms of dystocia and the associated
risk factors. Aboul-Fadle et al. (1993) have estimated the prevalence of dystocia as 9%; however,
Arthur (1992) and Tibary and Anoussai (1997) have reported relatively lower incidences (2 to
5%).
Dystocia has been found to have a profound effect on survival of the dam and fetus. In horses,
survival rate of mares at discharge ranged between 84% and 96%, while that of the foals was
low, between 10% and 35% (Byron et al., 2003; Carluccio et al., 2007; Norton et al., 2007). In
cattle, the survival rate of cows with dystocia ranged between 70% and 95% and that of the
calves was relatively high, between 40 and 70% (Noakes et al., 2009; Roberts, 2012). Dystocia
also has adverse effects on reproductive performance. The service interval, service period, days
open, and foaling/calving interval were found to be longer in mares or cows afflicted
with dystocia compared to normal parturient dams (Byron et al., 2003; Carluccio et al., 2007;
Gaafar et al., 2011; Abernathy-Young et al., 2012).
When physical investigation fails to provide a diagnosis in demanding cases, blood analysis may
benefit in ascertaining the problem. Assisted calving was found to cause important metabolic
changes in the dam and fetus (Vannucchi et al., 2015). The serum concentration of estradiol-
4
17beta increased with the calving difficulty score (Sorge et al., 2008). Cattle and buffaloes
suffering from dystocia, and especially those with uterine torsion were associated with hepatic
dysfunction; on the other hand, fetotomy had no effect on hepatocellular damage (Hussein and
Abd Ellah, 2008; Ali and Derar, 2015). In horses and cattle, acute phase proteins (serum amyloid
A [SAA] and haptoglobin [Hp]) are produced by the liver in response to inflammation, infection,
trauma and stress (Petersen et al., 2004; Chan et al., 2010; Canisso et al., 2014; Brodzki et al.,
2015a,b). No reports could be found dealing with the profile of acute-phase proteins during
dystocia in any animal species.
Studies on dystocia and the associated risks in camels, compared to other livestock, are very
limited. The aims of this study were to investigate the prevalence, forms and risks of dystocia in
the dromedary camel as well as the associated hematobiochemical changes.
2. Materials and methods
2.1. Survey for the prevalence of dystocia in two herd management systems
A herd-level questionnaire was used to gather information about the prevalence of dystocia in
dromedary camel herds (n = 95). In 61 herds, the camels (n = 3435) were left unconfined in open
desert areas (free system), while in the other 34 herds, the camels (n = 1893) were kept in pens
(intensive system, 15-20 m2/head, 10-15 heads/pen). The probability of anterior, posterior and
transverse presentations was included in this survey. Data were collected for the calving season
2014/2015. Camels in both management systems were fed mainly on alfalfa hay and barley
concentrate.
2.2. Obstetrical examination and animal classification
One hundred and seven female dromedary camels were presented at the Qassim Veterinary
Teaching Hospital due to severe dystocia (failure to progress in labor to the point of needing
human intervention). Of the dams, 9.3% (n = 10), 15% (n = 16), 15.9% (n = 17) and 59% (n =
64) arrived at the clinic within 24, 48, 72 and > 72 h of labor pain, respectively. All but five
females were at full term (12 to 13 mo of gestation). Two cases of uterine torsion were in the 8th
and 9th month of gestation, while three other cases were in the 11th month of pregnancy. The
dams showed signs of depression (46.7%, n = 50), lack of appetite and anorexia (88.8%, n = 95),
5
distress with frequent standing and sitting and repeated side-to-side rolling accompanied by
excessive straining (56.1%, n = 60), abnormal vaginal discharges (8.4%, n = 9) and diminishing
signs of parturition (6.5%, n = 7). Of the dams, 30.8% (n = 33) were primiparous and 69.2% (n =
74) multiparous.
On admission, the dams were examined per vagina for the adequacy of the soft and bony birth
ways for normal passage of the fetus. The fetus was examined for the presentation, position,
posture and viability. When it was difficult to reach the fetus, as in cases of vaginal adhesion or
narrowing/closure of the cervix or due to uterine torsion, the fetal viability was determined per-
rectum or after performing Cesarean section.
In cases of uterine torsion, clinical examinations included determining the degree of torsion
(mild: < 180º, moderate: 180° to 270°, high: > 270°), the direction of torsion from behind
position (clockwise or counter-clockwise) and the presence of vaginal involvement (pre- or
postcervical). The degree of torsion was determined vaginally (degree of twisting of vaginal
folds) and/or rectally (degree of tension on the broad ligaments) (Noakes et al., 2009; Roberts,
2012).
Dystocia was treated with traction (19.6%, n = 21), partial fetotomy (38.3%, n = 41) and
Cesarean section (33.6%, n = 36). Partial fetotomy (1-3 cuts) was carried out using a Thygesen
fetotome (Kruuse Embryotome Thygesen, 180011, Longeskov, Denmark). Cesarean section was
performed at the left paralumbar fossa (Elias, 1991). A few cases were treated with slow rolling
(2.8%, n = 3), administration of 25 mg PGF2 im (Dinoprost®, Lutalyse, Pharmacia & Upjohn,
NY, USA) (0.9%, n = 1) or euthanized due to poor health status (6.5%, n = 7).
2.3. Blood analysis
Before obstetrical handling, two jugular blood samples were collected from each animal, one on
EDTA and the other without an anticoagulant. A complete blood count was carried out on the
EDTA sample using the VetScan HM5 (Abaxis, CA, USA). The second blood sample was
centrifuged at 1200 × g for 10 min and the serum samples obtained were stored at -20 °C for
clinical chemical analysis. To serve as control, blood samples were collected from six female
6
dromedary camels during normal parturition. Serum concentrations of estradiol-17β (E2) and
progesterone (P4) were determined by ELISA using commercial kits (Human Gesellschaft fur
Biochemica und Diagnostica, Wiesbaden, Germany). The coefficient of variance (CV) was 4.8
and 8.1% and 5.9 and 8.4% for the intra- and interassay and the sensitivity of the assay was 3 pg/
mL−1 and 0.03 ng/ mL−1, respectively. Using kits provided by the Human mbH, the serum
samples were used to determine the serum concentrations of total protein, albumin, calcium,
phosphorus, magnesium, blood urea nitrogen (BUN) and creatinine. The serum activity of
aspartate aminotransferase (AST) was also estimated. A fully-automated open-system
biochemistry analyzer was used for the analysis (Biosystems A15, Spain).
The serum concentrations of Hp and SAA were determined as recently reported for application
in camels (Tharwat and Al-Sobayil, 2015). Haptoglobin was measured according to the
prevention of the hemoglobin peroxidase activity, which is directly proportional to the amount of
Hp (Tridelta Development Ltd., Ireland). The analytical sensitivity of the assay was 0.0005
mg/mL, and the intra- and inter-assay CVs were 5% and 6%, respectively. The SAA was
determined by a solid phase sandwich ELISA (Tridelta Development Ltd., Ireland). The
analytical sensitivity of the assay was 0.15 µg/mL and the intra- and inter-assay CVs were 4.5%
and 6%, respectively.
2.4. Statistical analysis
Logistic regression was performed to identify risk factors for the dependent variables. The
dependent variables were the fetal and maternal mortality, while the independent variables were
parity, duration of dystocia, causes of dystocia, and method of treatment. Prevalence of dystocia
in the free and intensive systems and in primi- and multipara were compared using the chi-square
test. The effect of dystocia duration on the blood parameters was determined using the analysis
of variance (ANOVA), with Fisher’s protected least significant difference (LSD) as the post-
ANOVA test. Data were analyzed using the IBM-SPSS program, version 19.0 (2010).
Significance level was set at P < 0.05.
3. Results
3.1. The prevalence of dystocia
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A total of 1890 calvings were recorded in the 95 camel herds, 1267 in the free system and 526 in
the intensive system. The overall prevalence of dystocia was 8.6% (163/1890). The risk of
occurrence of dystocia was higher in camels housed in intensive systems (12.6%, 66/526) than in
those in free systems (7.1%, 97/1267) (Odds ratio = 1.9, P = 0.0003) and higher in primipara
(11.4%, 54/472) than in multipara (7.2%, 109/1508) (Odds ratio = 1.7, P = 0.005). The
frequencies of anterior, posterior and transverse presentations were 98.1% (n = 1853), 1.6% (n =
31), 0.3% (n = 6), respectively.
3.2. Forms of dystocia
Abnormal posture represented the most common cause of dystocia (51.4%, 55/107) with no
significant differences between primi- and multipara (Table 1, Fig. 1 A,B,C). Head deviations
were mostly (26/28, 92.9%) accompanied by double carpal flexion. The incidences of anterior,
posterior and transverse presentations in these cases of dystocia were 71% (n = 71), 19% (n =
19) and 10% (n = 10), respectively.
Uterine torsion was the second most prevalent cause of dystocia, and was observed more
frequently in multi- than in primipara (P = 0.006) and mostly in clockwise (76%, 19/25)
direction. Uterine torsion was solely post-cervical with vaginal involvement (Fig. 1 D,E) and was
of mild (16%, n = 4), moderate (56%, n = 14) and high (28%, n = 7) degree. Vaginal adhesion
was observed in long-standing cases (16%, n = 4).
Feto-pelvic disproportion was noticed more frequently in primi- than in multipara (P = 0.008). It
included cases with fractured (n = 4) and narrow (n = 2) pelvises and in cases with over-sized (n
= 3) and emphysematous (n = 3) fetuses (Fig. 1 F,G).
Narrow cervix was observed in long-standing cases of dystocia (n = 4) and in premature births (n
= 3). Vaginal adhesions were noted in association with uterine torsion (n = 4), but were also seen
in cases with no torsion (n = 2). In the two cases of vaginal prolapse, the fetal head and forelimbs
had incorrectly presented through the prolapsed vagina (Fig. 1 H,I).
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Collectively, maternal and fetal dystocia were observed in frequencies of 43% (n = 46) and 57%
(n = 61), respectively, with no significant difference.
3.3. Risks associated with fetal and maternal mortalities
High fetal mortality (87.9%, 94/102) was observed, with 7.8% (n = 8) fetuses found alive, 31.4%
(n = 32) dead but not putrefied, and 60.8% (n = 62) putrefied/emphysematous. A significant
association was detected between fetal deaths and duration of dystocia (Odds ratio = 8.04, P =
0.005). Living fetuses were found in dams admitted to the clinic within 24 h (n = 6) or 48 h (n =
2) of labor pain. On the other hand, there were no relationships between parity, causes of
dystocia and fetal mortality (Table 2).
A relatively high incidence of dam mortality rate was recorded (17.8%, 19/102). Maternal deaths
occurred during obstetrical handling (21.1%, n = 4), and 24 h (31.6%, n = 6), 48 h (26.3%, n =
5), 72 h (10.5%, n = 2) or >72 h (10.5%, n = 2) after obstetrical operations. Significant
associations were detected between dam mortality rate and the duration of dystocia (Odds ratio =
4.74, P = 0.03) and fetal viability (Odds ratio = 5.82, P = 0.02) (Table 3). Maternal deaths
occurred mostly in those arriving to the clinic after 72 h of labor pain (16/19, 84.2%) and mainly
in those carrying emphysematous/putrefied fetuses (79%, 15/19). Maternal deaths were due to
toxemia (52.6%, n = 10), rupture of the uterus or cervix (15.8%, n = 3), uterine prolapse (5.3%, n
= 1) or to indefinite cause (26.3%, n = 5).
Post-operative complications included vaginal or vulvar lacerations (n = 13), retained placenta (n
= 8) and uterine prolapse (n = 4).
3.4. Changes in blood parameters
Increasing duration of dystocia was associated with significant (P < 0.05) increases in SAA, Hp,
BUN, and AST, but with decrease in E2 concentrations (Fig. 2, Table 4). The white blood cells
and neutrophils showed a transient increase followed by a significant decrease in their count (P <
0.05) (Table 5).
4. Discussion
9
Based on the present results, dystocia is a serious problem in dromedary camels, with
negative impact on dam and calf survivability. The overall prevalence of dystocia in
dromedary camels reported here (8.9%) and by others (9%, Aboul-Fadle et al., 1993) is
comparable to that reported in horses (4 - 10%, [Vandeplassche, 1993; McCue and Ferris,
2012]) and in cattle (4 - 13%, [Noakes et al., 2009; Roberts, 2012]). Earlier and recent
reports have concurred that dystocia occurs more frequently in primipara than in
multipara (Nix et al., 1998; Gaafar et al., 2011; Roberts, 2012), supporting the present
findings. Immaturity of the dam at the time of breeding and mating with incompatibly
larger males can be considered as causes for the higher incidence of dystocia in
primipara.
Insufficient exercise and mobility and psychological stress may be predisposing factors in
the higher dystocia rate of camels in intensive management systems. In addition, in
intensive systems, the distress and injuries related with dystocia in individual animals
will attract less attention (Mee, 2008; Mee et al., 2013). Higher dystocia rates in dairy
cows have been reported in tie stall housing (Mee et al., 2013). Moreover, confinement in
calving pens compared to a yard or pasture has been associated with increased dystocia in
cattle (Noakes et al., 1992).
Concerning the forms of dystocia, dromedary camels occupy a middle position between
horses and cattle. Due to the long neck and extremities, postural abnormalities are the
most common forms of dystocia in dromedary camels; this is similar to the condition in
horses (Vandeplassche, 1987; Frazer et al., 1996; Noakes et al., 2009; Yorke et al., 2012).
On the other hand, unlike horses, incidence of uterine torsion seems to be substantially
higher in camels than in cattle (Noakes et al., 2009; Ali et al., 2011; Roberts, 2012).
The frequency of posterior and transverse presentations during dystocia was greater than
that observed during spontaneous parturitions. This would suggest that posterior and
transverse presentations are important causes of fetal malformation and dystocia. The
same assumption has been reported by Vandeplassche (1987) for mares, where the
fetuses were in anterior, posterior and transverse presentations in incidences of 99%, 1%
10
and 0.1% during spontaneous parturitions and in incidences of 68%, 16% and 8% in
severe dystocia, respectively.
Uterine torsion was the most common cause of dystocia of maternal origin in dromedary camels,
most being of moderate and high degrees. Several reports have supported the concept that active
movements by a large fetus during late gestation and the early stage of labor might precipitate
rotation of the unstable uterus (Baker, 1988; Frazer et al., 1996; Noakes et al., 2009). Decreased
amniotic fluid in relation to the size of the fetus and uterus has been suggested as a very plausible
explanation for the selective occurrence of uterine torsion in cows (Schonfelder and Sobiraj,
2005). Uterine torsion has been reported in a few cases in camels (Nigam et al., 1977; Aboul-
Fadle et al., 1993; Bolbol et al., 1993), but the symptoms of uterine torsion are not clear for most
camel owners and are confused with other medical problems like colic and/or indigestion.
Therefore, in many instances, the diagnosis is delayed, thus threating the life of the fetus and
dam.
The period between the onset of dystocia and its resolution has an important bearing on
fetal outcome. In addition, dystocia duration and fetal viability have determinable effects
on dam survival. With diffuse placenta in camels, placental separation is rapid, leading to
fetal anoxia and death (Ali and Derar, 2015). Similarly, increased duration of the second
stage of labor in the horse affected fetal outcome negatively (Norton et al., 2007).
Perinatal asphyxia associated with dystocia was one of the two leading causes for equine
reproductive loss in the central Kentucky area (Hong et al., 1993). A slight calving
problem increased the odds of abortion by 2.91 in heifers and 4.67 in multiparous cows;
50% of fetal deaths were a direct result of dystocia (Meyer et al., 2001). Very early
referral of camels with dystocia to treatment centers may improve fetal and maternal
outcomes. Dystocia should be suspected in dromedary camels when the second stage of
labor exceeds two hours and/or when the dam shows frequent signs of distress with
frequent standing and sitting accompanied by frequent side-to-side rolling (Tibary and
Anouassi, 1997).
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In the current study, dystocia was associated with elevation of the acute-phase proteins (SAA
and Hp). The hepatic biosynthesis of SAA is up-regulated by pro-inflammatory cytokines, and
circulating concentrations can be increased by up to 1000-fold (Uhlar and Whitehead, 1992;
Jensen and Whitehead, 1998). Chronically elevated SAA concentrations are a prerequisite for the
pathogenesis of secondary amyloidosis, a progressive and fatal disease characterized by the
deposition in major organs (liver, kidney, spleen) of insoluble plaques composed principally of
proteolytically cleaved SAA (Urieli-Shoval et al., 2000; Brodzki et al., 2015a,b). In mares,
concentrations of SAA and Hp rapidly increased subsequent to experimental induction of
placentitis and remained increased until abortion (Canisso et al., 2014); in postpartum cows,
increased SAA and Hp levels have been used to recognize uterine infection (Chan et al., 2010).
Elevated concentrations of acute phase proteins have also been detected in cows with pyometra
and in cows with subclinical endometritis (Brodzki et al., 2015a,b).
Female camels with dystocia also differed from the controls in an increase in concentrations of
AST and BUN, probably due to tissue trauma. Aspartate aminotransferase is an enzyme
associated with liver parenchymal cells; it is elevated in acute liver damage as well as in cardiac
and skeletal muscle damages (Thrall et al., 2012). Increased BUN may be due to muscle
decompensation, acute glomerulonephritis, nephrosclerosis, and tubular necrosis (Thrall et al.,
2012). Transient elevation in the total leukocyte and neutrophil counts occur in most infections
and tissue damage. A final drop in the total leukocytic and neutrophil counts is a sign of toxemia
due to fetal death and putrefaction (Harvey, 2012). Loss of the placental function with increasing
duration of dystocia might be the cause of decreasing E2 concentration (Tharwat et al., 2015).
Contradictory findings concerning estradiol concentration in relation to dystocia have been
reported by Sorge et al. (2008). The authors found primary positive relation of estradiol
concentration to birth weight and male sex of the fetus (frequent causes of dystocia in heifers),
therefore high estradiol also related to dystocia was recorded in this study.
5. Conclusions
Dystocia is a serious problem in dromedary camels and has a negative impact on fetal and
maternal survivability. In this study, it was observed more frequently in intensive than in free
systems. Postural abnormalities were the most common forms of dystocia, with uterine torsion
12
being the most common cause of dystocia of maternal origin. Dystocia was associated with high
fetal mortality. The period between the onset of dystocia and its resolution had an important
bearing on fetal and maternal outcomes. Increasing duration of dystocia was associated with
changes in some hematological and biochemical parameters, especially the acute-phase proteins,
AST and BUN, indicating acute inflammation, severe tissue damage and hepato-renal
dysfunction. The effect of dystocia and methods of treatment on the postpartum reproductive
performance should be further investigated.
There is no conflicted of interest
Acknowledgments
The authors would like to thank Mohammed W. Arafah and Mohammed S. Alnakhli, students in
the Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine,
Qassim University, Kingdom of Saudi Arabia, for their kind support during data collection.
Appreciation is extended to Nuriye Peachy (Professor of English), Qassim University, for editing
the manuscript for English language. This study was supported by the Deanship for Scientific
Research, Qassim University, Saudi Arabia.
References
Abernathy-Young, K.K., LeBlanc, M.M., Embertson, R.M., Pierce, S.W., Stromberg, A.J., 2012.
Survival rates of mares and foals and postoperative complications and fertility of mares after
cesarean section: 95 cases (1986-2000). J. Am. Vet. Med. Assoc. 241, 927-34.
Aboul-Fadle, W., Al-Eknah, M.M., Bolbol, A., Dafalla, A.E., Bendari, M., Al-Bisher, B.E.,
1993. Maternal dystocia in the female camels (Camelus dromedaries). Second scientific congress
of Egyptian Society for cattle disease. pp.90-97, 5-7 Dec., Assiut University, Egypt.
Ali, A., Derar, R., 2015. Comparative Theriogenology. Qassim University, Saudi Arabia, ISBN
978-603-8176-13-9. Pp 225-229
13
Ali, A., Derar, R.., Hussein, H.A., Abd Ellah, M.R., Abdel-Razek, A.K.h., 2011. Clinical,
hematological, and biochemical findings of uterine torsion in buffaloes (Bubalus bubalis). Anim.
Reprod. Sci. 126, 168-172.
Arthur, G.H., 1992. An overview of reproduction in the camelids. Proceedings of the First
International Camel Conference, Dubai, UAE. pp. 109-113.
Baker, I., 1988. Torsion of the uterus in the cow. In Practice. 10, 26. doi:10.1136/inpract.10.1.26
Bolbol, A.E., Al-Eknah, M.M., Aboul-Fadle, W., Ramadan, O., Bendari, M., Al-Bisher, B.,
1993. Caesarean section in female camels. 2nd Sci. Cong. Egyptian Society for cattle disease. pp.
82-89, 5-7 Dec., Assiut University, Egypt.
Brodzki, P., Kostro, K., Brodzki, A., Ziętek, J., 2015a. The concentrations of inflammatory
cytokines and acute-phase proteins in the peripheral blood and uterine washings in cows with
pyometra. Reprod. Domest. Anim. 50, 417-22.
Brodzki, P., Kostro, K., Krakowski, L., Marczuk, J., 2015b. Inflammatory cytokine and acute
phase protein concentrations in the peripheral blood and uterine washings of cows with
subclinical endometritis in the late postpartum period. Vet. Res. Commun. 39, 143-149.
Byron, C.R., Embertson, R.M., Bernard, W.V., Hance, S.R., Bramlage, L.R., Hopper, S.A.,
2003. Dystocia in a referral hospital setting: approach and results. Equine Vet. J. 35, 82-85.
Canisso, I.F., Ball, B.A., Cray, C., Williams, N.M., Scoggin, K.E., Davolli, G.M., Squires,
E.L., Troedsson, M.H., 2014. Serum amyloid A and haptoglobin concentrations are increased in
plasma of mares with ascending placentitis in the absence of changes in peripheral leukocyte
counts or fibrinogen concentration. Am. J. Reprod. Immunol. 72, 376-85.
14
Carluccio, A., Contri, A., Tosi, U., De Amicis, I., De Fanti, C., 2007. Survival rate and short-
term fertility rate associated with the use of fetotomy for resolution of dystocia in mares: 72
cases (1991-2005). J. Am. Vet. Med. Assoc. 230, 1502-1505.
Chan, J.P., Chang, C.C., Hsu, W.L., Liu, W.B., Chen, T.H., 2010. Association of increased
serum acute-phase protein concentrations with reproductive performance in dairy cows with
postpartum metritis. Vet. Clin. Pathol. 39, 72-8.
Elias, E., 1991. Left ventrolateral cesarean section in three dromedary camels (Camelus
dromedarius). Vet. Surg. 20, 323-325.
Frazer, G.S., Perkins, N.R., Constable, P.D., 1996. Bovine uterine torsion: 164 hospital referral
cases. Theriogenology 46, 739-758.
Gaafar, H.M., Shamiah, Sh.M., El-Hamd, M.A., Shitta, A.A., El-Din, M.A., 2011. Dystocia in
Friesian cows and its effects on postpartum reproductive performance and milk production. Trop.
Anim. Health. Prod. 43, 229-34.
Harvey, J.W., 2012. Veterinary Hematology: A Diagnostic Guide and Color Atlas. Elsevier-
Saunders, Missouri, USA.
Hong, C.B., Donahue, J.M., Giles, R.C., Petrites-Murphy, M.B., Poonacha, K.B., Roberts, A.W.,
Smith, B.J., Tramontin, R.R., Tuttle, P.A., Swerczek, T.W., 1993. Equine abortion and stillbirth
in central Kentucky during 1988 and 1989 foaling seasons. J. Vet. Diag. Invest. 5, 560-566.
Hussein, H., Abd Ellah, M.R., 2008. Effects of dystocia, fetotomy and caesarian sections on the
liver enzymes activities and concentrations of some serum biochemical parameters in dairy
cattle. Anim. Reprod. Sci. 105, 384-391.
IBM SPSS., 2010. Statistics for Windows, Version 19.0. Armonk, NY: IBM Corp.
15
Jensen, L.E., Whitehead, A.S., 1998. Regulation of serum amyloid A protein expression during
the acute-phase response. Biochem. J. 334, 489-503.
McCue, P.M., Ferris, R.A., 2012. Parturition, dystocia and foal survival: a retrospective study of
1047 births. Equine Vet. J. Suppl. s41, 22-25.
Mee, J.F., 2008. Prevalence and risk factors for dystocia in dairy cattle: A review. Vet. J. 176,
93-101.
Mee, J.F., 2012. Prevalence and Risk Factors for Dystocia in Dairy Cattle-With Emphasis on
Confinement Systems. WCDS Advances in Dairy Technology 24, 113-125.
Mee, J.F., Grant, J., Sánchez-Miguel, C., Doherty, M., 2013. Pre-Calving and Calving
Management Practices in Dairy Herds with a History of High or Low Bovine Perinatal Mortality.
Animals (Basel) 3, 866-881.
Meyer, C.L., Berger, P.J., Koehler, K.J., Thompson, J.R., Sattler, C.G., 2001. Phenotypic trends
in incidence of stillbirth for Holsteins in the United States. J. Dairy Sci. 84, 515-523.
Nigam, J.M., Gupta, R.C., Khar, S.K., Shetty, B.R., 1977. Torsion of the uterus in a Camel. The
Haryana Vet. 116, 33-36.
Nix, J.M., Spitzer, J.C., Grimes, L.W., Burns, G.L., Plyler, B.B., 1998. A retrospective analysis
of factors contributing to calf mortality and dystocia in beef cattle. Theriogenology 49, 1515-
1523.
Noakes, J., Allen, O., Martin, W.S., Alves, D., 1992. Patterns of stillbirth and dystocia in Ontario
cow-calf herds. Can. J. Vet. Res. 56, 47-55.
Noakes, D.E., Parkinson, T.J., England, G.C.W., 2009. Veterinary Reproduction and Obstetrics.
Ninth ed. Saunders- Elsevier, Zhejiang, China.
16
Norton, J.L., Dallap, B.L., Johnston, J.K., Palmer, J.E., Sertich, P.L., Boston, R., Wilkins, P.A.,
2007. Retrospective study of dystocia in mares at a referral hospital. Equine Vet. J. 39, 37-41.
Petersen, H.H., Nielsen, J.P., Heegaard, P.M., 2004. Application of acute phase protein
measurements in veterinary clinical chemistry. Vet. Res. 35, 163-187.
Roberts, S.J., 2012. Veterinary obstetrics and genital diseases. Montana, USA: Literary
Licensing, LLC.
Schonfelder, A., Sobiraj, A., 2005. Etiology of torsio uteri in cattle: a review Schweiz Arch
Tierheilkd. 147, 397-402.
Sorge, U.S., Kelton, D.F., Staufenbiel, R. 2008. Prepartal concentration of estradiol-17beta in
heifers with stillborn calves. J. Dairy Sci. 91, 1433-7.
Tenhagen, B.A., Helmbold, A,, Heuwieser, W., 2007. Effect of various degrees of dystocia in
dairy cattle on calf viability, milk production, fertility and culling. J. Vet. Med. A. Physiol.
Pathol. Clin. Med. 54, 98-102.
Tharwat, M., Ali, A., Al-Sobayil, F., Selim, L., Abbas, H., 2015. Haematobiochemical profile in
female camels (Camelus dromedarius) during the peripaturient period. J. Camel Prac. Res. 22,
101-106.
Tharwat, M., Al-Sobayil, F., 2015. The impact of racing on serum concentrations of acute phase
proteins in racing dromedary camels. Comp. Clin. Pathol. 24, 575-579.
Thrall, M.A., Weise, G., Allison, R., Campbell, T.W., 2012. Veterinary Hematology and Clinical
Chemistry. Second edition, Oxford, UK.
17
Tibary, A., Anouassi, A., 1997. Anatomy, physiology, BSE, pathology and artificial breeding.
In: Theriogenology in Camelidae. Actes Editions: Institut Agronomique et Vétérinaire Hassan II,
Rabat.
Uematsu, M., Sasaki, Y., Kitahara, G., Sameshima, H., Osawa, T., 2013. Risk factors for
stillbirth and dystocia in Japanese Black cattle. Vet. J. 198, 212-216.
Uhlar, C.M., Whitehead, A.S., 1992. Serum amyloid A, the major vertebrate acute-phase
reactant. Eur. J. Biochem. 265, 501-523.
Urieli-Shoval, S., Linke, R.P., Matzner, Y., 2000. Expression and function of serum amyloid A,
a major acute-phase protein, in normal and disease states. Curr. Opin. Hematol. 7, 64-69.
Vandeplassche, M.M., 1987. The pathogenesis of dystocia and fetal malformation in the horse. J.
Reprod. Fertil. Suppl. 35, 547-552.
Vandeplassche, M., 1993. Dystocia, In: McKinnon, A., Voss, J. (Eds), Equine Reproduction. Lea
and Febiger, Philadelphia, pp. 578 -587.
Vannucchi, C.I., Rodrigues, J.A., Silva, L.C., Lúcio, C.F., Veiga, G.A., Furtado, P.V., Oliveira,
C.A., Nichi, M., 2015. Association between birth conditions and glucose and cortisol profiles of
periparturient dairy cows and neonatal calves. Vet. Rec. 176, 358.
Yorke, E.H., Caldwell, F.J., Johnson, A.K., 2012. Uterine torsion in mares. Compend. Contin.
Educ. Vet. 34, E2.
18
Figures
Figure 1. Forms of dystocia in dromedary camels: (A) lateral deviation of the head; (B) double
shoulder flexion; (C) double hip flexion (breech presentation); (D,E) high degree of uterine
torsion; (F) feto-pelvic disproportion due to fracture of the left ilium; (G) emphysematous fetus;
(H,I) fetus incorrectly presented through a prolapsed vagina.
19
Figure 2. Concentrations (mean ± SD) of serum amyloid A and haptoglobin in relation to the
duration of dystocia (control, n = 6; 24 h, n =10; 48 h, n = 16; 72 h, n = 17; >72 h, n = 64) in
dromedary camels.
20
Table 1. Frequency of different forms of dystocia in primi- and multiparous dromedary camels
(n = 107).
Forms Frequency n (%)
Primiparous Multiparous P value
Head deviation (n=28) 10 (30.3)a 18 (24.3)a 0.1
Uterine torsion (n=25) 2 (6.1)a 23 (31.1)b 0.006
Feto-pelvic disproportion (n=12) 8 (24.2)a 4 (5.4)b 0.008
Transverse presentation (n=10) 4 (12.1)a 6 (8.1)a 0.7
Hip flexion (n=8) 6 (18.2)a 2 (2.7)b 0.06
Hock flexion (n=7) 2 (6.1)a 5 (6.8)a 1.0
Narrow cervix (n=7) 0.0 (0.0)a 7 (9.5)a 0.1
Vaginal adhesion (n=6) 0.0 (0.0)a 6 (8.1)a 0.2
Vaginal prolapse (n=2) 0.0 (0.0)a 2 (2.7)a 1.0
Shoulder flexion (n=1) 1 (3)a 0.0 (0.0)a 1.0
Dog-sitting position (n=1) 0.0 (0.0)a 1 (1.4)a 1.0
Total (n=107) 33 74
a,bValues with different letters differ significantly.
21
Table 2. Logistic regression model for risk factors associated with fetal mortality during dystocia
in dromedary camels.
Variables β SE Odds P value 95% CI
Parity 0.777 1.147 0.460 0.498 0.230-20.586
Duration of dystocia 0.966 0.341 8.036 0.005 1.347-5.124
Cause 1.278 1.029 1.542 0.214 0.477-26.998
Constant -3.500 3.295 1.128 0.288
Β: Regression coefficient; SE: standard error; CI: confidence interval.
Parity: primi- (n=26) vs multipara (n=81); Duration of dystocia: 24h (n=10) vs 48h (n=16) vs
72h (n=17) vs >72h (n=64); Cause: maternal (n=46) vs fetal (n=61).
22
Table 3. Logistic regression model for risk factors associated with dam mortality during or
following dystocia in dromedary camels.
Variables β SE Odds P 95% CI
Parity 0.488 0.732 0.444 0.505 0.388 -0.6841
Duration of dystocia 1.099 0.505 4.741 0.029 1.116 -0.8072
Cause 0.515 0.647 0.633 0.426 0.471 -0.5953
Treatment -0.018 0.403 0.002 0.965 0.528 -0.2163
Fetus -2.897 1.201 5.816 0.016 0.042 -0.581
Constant -1.540 2.927 0.277 0.599
Β: Regression coefficient; SE: standard error; CI: confidence interval.
Fetus: alive (n=8) vs dead (n=94).
23
Table 4. Effect of dystocia duration on blood biochemistry (mean ± SD) of dromedary camels.
Parameters Duration of dystocia P
Value Control, n=6 24h, n=10 48h, n=16 72h, n=17 >72h, n=64
Estradiol 17β pg/mL 1793±1295.1a 804.5±177.33b 41.43±21c 43.33±16.5c 28.33±19.29c 0.001
Progesterone ng/mL 0.65±0.33a 1.83±0.86a 1.73±0.78a 1.53±0.68a 0.87±0.26a 0.6
Total protein g/dL 4.81±3.2a 4.59±3.1a 7.39±1.11a 6.3±0.58a 8.2±0.69a 0.2
Albumin g/dL 2.95±1.56a 3.14±1.45a 4.32±0.85a 3.79±0.56a 3.88±0.55a 0.3
Triglycerides mg/dL 40.14±2.85a 51.75±10.3a 52.43±16.79a 62.33±13.57a 40±5.1a 0.1
Cholestrol mg/dL 76.03±9.76a 54.92±13.1a 58.51±17.5a 51.33±11.1a 68.70±18.75a 0.1
Calcium mg/dL 8.11±0.15a 9.46±2.34a 8.23±0.23a 8.37±0.20a 8.2±0.34a 0.4
Phosphorus mg/dL 7.11±0.59a 7.26±0.62a 7.87±1.2a 7.43±1.25a 8.83±1.13a 0.2
Magnesium mg/dL 2.33±0.2a 2.35±0.19a 2.4±0.2a 2.46±0.22a 2.38±0.16a 0.9
BUN mg/dL 8.79±1.18a 20.14±15.18ab 51.53±39.27bc 50.47±0.17bc 45.63±27.65bc 0.03
AST u/L 3.20±2.92a 3.84±2.55a 5.7±4.83ab 7±4.66ab 10.5±5.7bc 0.04
Creatinine md/dL 1.23±0.37a 1.98±1.01a 1.6±0.35a 1.47±0.29a 1.57±0.26a 0.4
BUN: blood urea nitrogen; AST: aspartate aminotransferase. A,b,c:Values with different letter in
the same raw differ significantly.
24
Table 5. Effect of dystocia duration on the hemogram (mean ± SD) of dromedary camels.
Parameters Duration of dystocia P Value
Control, n=6 24h, n=10 48h, n=16 72h, n=17 >72h, n=64
WBC (x109/L) 17.94±7.34a 18.41±8.53a 34.82±2.45b 22.23±11.82ab 5.66±2.63c 0.006
NEU (x109/L) 14.97±6.99a 14.36±8.52a 30.44±1.63b 18.12±7.87a 3.67±1.34c 0.005
LYM (x109/L) 1.7±0.69a 2.4±0.68a 2.58±0.82a 2.43±6.91a 1.64±1.24a 0.08
MON (x109/L) 0.64±0.81a 0.74±0.92a 0.49±0.12a 0.78±0.57a 0.33±0.23a 0.1
EOS (x109/L) 0.51±0.7a 0.7±0.4a 1.3±0.5a 0.9±0.3a 0.3±0.4a 0.5
BAS (x109/L) 0.001±0.01a 0.002±0.01a 0.002±0.01a 0.002±0.01a 0.001±0.01a 0.9
RBC (x1012/L) 9.57±2.07a 9.37±1.06a 10.03±0.66a 10.29±1.38a 9.93±1.47a 0.9
HGB (g/L) 13.94±2.14a 13.73±0.75a 17.4±1.63a 16.28±2.14a 13.54±3.36a 0.1
HCT (%) 24.55±4.31a 24.51±2.47a 28.44±1.25a 29.09±4.01a 27.12±5.03a 0.3
MCV (fl) 25.75±2.49a 26±2.45a 28±0.82a 28.5±0.76a 27.4±0.80a 0.8
MCH (pg) 14.8±1.21a 14.8±1.2a 18.6±0.82a 16.68±1.96a 13.5±1.78a 0.5
MCHC (g/dL) 57.18±3.13a 56.27±2.61a 67.33±1.7a 58.82±7.41a 49.64±6.67a 0.2
PLT (x109/L) 246.88±63.74a 231±70.1a 300±8.58a 221.5±71.01a 239.4±47.66a 0.7
WBC: white blood cells; NEU: neutrophils; LYM: lymphocytes; MON: monocytes; EOS:
Eosinophils; BAS: basophiles;RBS: red blood cells; HGB: hemoglobin: HCT: hematocrit; MCV:
mean corpuscular volume; MCH: mean corpuscular hemoglobin ; MCHC: mean corpuscular
hemoglobin concentration; PLT: platelet count.
a,b,c Values with different letter in the same raw differ significantly.