Theriogenology 85 (2016) 1576–1581

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Theriogenology
journal homepage: www.theriojournal.com

Phimosis in male dromedary camels: Clinical findings and

changes in the hemogram, nitric oxide metabolites, and
testosterone concentrations
Ahmed Ali a, b, *, Derar Derar a, b, Fahd A. Al-Sobyil a, Moustafa M. Zeitoun c,
Khaled M.A. Hassanein d, Abdella Al-Howas a
a
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Qassim University, Qassim, Saudi Arabia
b
Faculty of Veterinary Medicine, Department of Theriogenology, Assiut University, Assiut, Egypt
c
Department of Animal production, College of Agriculture and Veterinary Medicine, Qassim University, Qassim, Saudi Arabia
d
Faculty of Veterinary Medicine, Department of Pathology, Assiut University, Assiut, Egypt

a r t i c l e i n f o a b s t r a c t

Article history: The objectives of this study were to elucidate the clinical findings in male dromedary camels
Received 26 July 2015 with phimosis (PHI, n ¼ 43) and to investigate the association of this syndrome with the
Received in revised form 11 January 2016 hemogram, nitric oxide metabolites (NOMs), and testosterone concentrations. History and
Accepted 12 January 2016
signalment were obtained, and a breeding soundness examination was performed. The
penis was exteriorized after administration of a pudendal nerve block. Abnormal masses
Keywords:
obtained from the prepuce and penis were prepared for histopathology. Blood samples for
Male dromedary camel
hemogram assessment were taken from the diseased animals and from 10 healthy control
Phimosis
Nitric oxide males. Total nitrates/nitrites were determined in sera using the Griess assay. Testosterone
Testosterone was estimated in sera using ELISA. Phimosis associated with detectable pathologic lesions,
mainly including ulcerative posthitis and lacerated glans penis, was present in 34 (79.1%) of
the 43 cases (PHI-P), whereas the remaining nine (20.9%) of the 43 cases had no noticeable
lesions (PHI-N). The PHI-P group showed higher leukocyte counts (P ¼ 0.001), especially
neutrophils (P ¼ 0.0001), and greater NOM concentrations (P ¼ 0.002) than the PHI-N and
control groups. However, testosterone concentrations did not differ among groups. In
conclusion, PHI in the male dromedary camels was mainly associated with ulcerative
posthitis and laceration of the glans penis. The presence of pathologic lesions in cases with
PHI was associated with leukocytosis, neutrophilia, and high NOM concentrations.
Ó 2016 Elsevier Inc. All rights reserved.

1. Introduction incomplete at the time of intromission [2]. In severe cases,

Erection of the penis in males with a sigmoid flexure as
seen in male camels, bulls, rams, and bucks depends on the
relaxation of the retractor muscle of the penis and the
pumping of blood into the corpus cavernosum penis [1].
When the relaxation is insufficient, the penile extension is
This study was conducted at Veterinary Teaching Hospital, Department
of Veterinary Medicine, Faculty of Agriculture and Veterinary Medicine,
Qassim University, Saudi Arabia.
* Corresponding author. Tel.: þ966 16 3801480; fax: þ966 16 3801360.
E-mail address: ahmedali77@hotmail.com (A. Ali).
this can lead to complete retention of the penis (phimosis,
PHI). Preputial stenosis, penile adhesions, hematomas,
peripreputial abscesses, and insufficient penile length have
been reported as causes of PHI [2–4].
Blood is supplied from the distal end of the crura to the
corpus cavernosum penis by two large vessels [5]. On
sexual stimulation, active rhythmic contractions of the
ischiocavernosus muscles force blood from the crura into
the dorsal canal and subsequently into the cavernous
spaces of the corpus cavernosum penis. The ischioca-
vernosus muscle contractions also cause occlusion of the
small, thin-walled crural veins that drain blood from the

0093-691X/$ – see front matter Ó 2016 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.theriogenology.2016.01.011
 A. Ali et al. / Theriogenology 85 (2016) 1576–1581 1577

corpus cavernosum penis. Thus, intracorporeal blood
pressure rapidly increases and full erection is attained [1].
Stimulation of the nervous system also leads to the secre-
tion of nitric oxide (NO), which causes the relaxation of the
smooth muscles of the corpora cavernosa [6]. In addition,
adequate concentrations of testosterone and an intact pi-
tuitary gland are required for the development of a healthy
erectile system [6,7].
There are limited reports on the pathology of the male
reproductive organs in Camelidae. Phimosis has most often
been described as an idiopathic process, the result of a
congenital small preputial opening, or the presence of le-
sions preventing exteriorization of the penis. The aim of
this study was to document the clinical findings associated
with cases of PHI and to investigate the association of
hemogram, serum nitric oxide metabolites (NOMs), and
testosterone concentrations with this condition in male
dromedary camels.
2. Materials and methods
2.1. Animals
was administered using a 16-gauge needle in both sides at a
point located lateral to the sacral region 12 cm cranial to the
base of the tail and 7 cm lateral to the midline. The animal
was then secured in lateral recumbancy for exploration of
the prepuce and penis. Using a blunt metal rod, the prepuce
was examined for injuries, lesions, swelling, edema and
patency of the preputial orifice, and cavity. For safe explo-
ration of the penis, long, blunt, bandage-wrapped forceps
were used. Attempts were made to exteriorize the penis
completely by unfolding the preputial layers. According to
the clinical findings, the camels with PHI were subdivided
into those with (PHI-P, n ¼ 34) or without (PHI-N, n ¼ 9)
detectable pathologic lesions.
2.3. Histopathology
Tissue specimens were obtained from tumor-like
structures at the tip of the prepuce in one animal and
from a peri-penile swelling on the dorsum of the glans
penis of another. The tissues were prepared for histologic
examination by standard technique and stained with
Hematoxline and Eosin [12].

Male dromedary camels with a history of phimosis (PHI, 2.4. Hematology

inability to extend the penis from the preputial sheath,
n ¼ 43) were included in this study. The history and
signalment including age, duration of condition, libido,
mating ability, previous fertility, and illness or injury were
recorded for each animal. The duration of the infertility
problems ranged from one to 8 months. The males were
aged between 6 and 16 years and weighed between 487 and
580 kg, with body condition scores (scale: 1–5) ranging
from 3 to 4 [8]. The camels were examined at the Veterinary
Teaching Hospital of Qassim University, KSA, during the
rutting season (September to March). Most of the animals
were left unconfined in open desert areas and fed mainly on
alfalfa hay and barley concentrate. The number of males to
females during the rutting season ranged from 1:15 to 1:25.
Ten male dromedary camels with normal fertility were used
as controls to compare the variations in blood parameters.
2.2. Breeding soundness examination
Between 10 AM and 12 AM, two blood samples were
drawn from the jugular vein of each animal before seda-
tion, one in EDTA and the other in tubes containing no anti-
coagulant for serum harvesting. Within 30 minutes of
collection, the whole blood sample was used for estimation
of complete blood count using the VetScan HM5 (Abaxis,
CA, USA). The serum from the other tube was separated by
centrifugation for 10 minutes at 1200  g and immediately
frozen for future analysis.
2.5. Nitrate/nitrite assay
The serum concentrations of total nitrates and nitrites
were determined colorimetrically using the Griess assay as
described by the manufacture (Sigma–Aldrich Co., MO,
USA). The Griess assay mechanism is summarized as the
azo coupling between diazonium species, which are

A breeding soundness examination was carried out as

previously described [9]. Briefly, the males were restrained Table 1
Clinical findings in male dromedary camels with phimosis (PHI, n ¼ 43).
in sternal recumbancy, and a general physical examination
was performed. The testes and epididymides were evalu- Clinical findings Frequency n (%)
ated for size and consistency using visual inspection, Testicular and scrotal affections
palpation, calipers, and ultrasound. On the basis of refer- Large testicles 3 (7)
ence values for male dromedary camels [10], the testes Large testicles with hematocele 2 (4.7)
Hydrocele -
were classified as small (<6  3  3 cm), normal (6–9  3– Preputial and penile affections
4  3–4 cm), and large (>9  4  4 cm) according to di- Posthitis 12 (27.9)
mensions of length, breadth, and depth, respectively. The Lacerated glans penis 4 (9.3)
internal genitalia were examined per rectum by ultraso- Preputial edema 3 (7)
Preputial adhesion 2 (4.7)
nography using a B-mode scanner equipped with a 5-MHz
Congenital narrow preputial orifice 2 (4.7)
linear-array transducer (Aloka SSD-500; Aloka Co., Ltd., Balanitis 2 (4.7)
Tokyo, Japan). The camels were then sedated with xylazine Preputial abscess 1 (2.3)
HCl Bomazine 10% (BOMAC Laboratories Ltd., New Zealand) Preputial squamous cell carcinoma 1 (2.3)
0.3 mg/kg body weight, intravenous. For examination of the Penile fat necrosis 1 (2.3)
Preputial prolapse 1 (2.3)
prepuce and penis, a pudendal nerve block was applied Apparently normal 9 (20.9)
[11]. Lidocaine 2% (w30 mL; Norbrook Laboratories, UK)
1578 A. Ali et al. / Theriogenology 85 (2016) 1576–1581

produced from sulfanilamide with NO2 (Griess reagents A
dye), and naphthylethylenediamine (Griess reagents B
dye). The assay kit contains these colorimetric dyes (A and
B), a nitrate reductase, an enzyme cofactor, buffer solution,
and NO2 and NO3 solutions as standard (0–100 mM). The
intra-assay and interassay coefficients of variation for the
NOM assay were 4.3% and 14.6%, respectively.
2.7. Statistical analysis
Data are presented as means  standard error of the
mean, and the analysis was conducted using the SPSS-
program, version 18.0 [13]. Differences among groups
were evaluated by analysis of variance. The level of signif-
icance was set at P < 0.05.

2.6. Testosterone assay

The serum testosterone was determined using the ELISA
technique according to the manufacturer’s instructions
(Human Geselschaft fur Biochemica and Diagnostica mbH,
Wiesbaden, Germany). Briefly, the assay is on the basis of
competitive interaction of testosterone and the hormone-
enzyme conjugate for a limited number of anti-
testosterone antibodies. Thus, the amount of the bound
hormone-enzyme conjugate is inversely proportional to
the concentration of testosterone in the serum. The intra-
assay and interassay coefficients of variation for the
testosterone were 3.7 and 8.4%, respectively.
3. Results
Most of the camels with PHI (41/43, 95.3%) had a pre-
vious history of successful mating (secondary PHI),
whereas only two cases had never served successfully
before (primary PHI). About two-thirds of the camels with
PHI (27/43, 67.4%) showed defects in the penis and prepuce,
with ulcerative posthitis and laceration of the glans penis
being the most common lesions. Ulcerative posthitis was
mostly (10/12) observed at the muco-cutaneous junction
between the outer layer (reflection) of the prepuce and the
skin (Table 1, Fig. 1A–C).

Fig. 1. Pathologic lesions associated with phimosis in male dromedary camels: (A) Ulcerative posthitis; (B) Balanitis with lacerated galea glandis; (C) Laceration of
the glans penis. Preputial squamous cell carcinoma in a male camel showing: (D) Preputial ulceration; (E) Nests showing the characteristics of various degrees of
keratinization (arrow; HE  100); (F) Neoplastic cells exhibiting pleomorphic, rounded shape with rare mitotic features (HE  400). Penile fat necrosis in a male
camel revealing: (G) Firm structure, having two holes filled with waxy material, removed from the dorsum of the glans penis; (H) and (I) Amorphous mass of
necrotic material (arrow) resulting from necrotic fat cells after the loss of their nuclei and cytoplasm (HE  100 and  200, respectively). A high-resolution
version of this slide for use with the Virtual Microscope is available as eSlide: VM02476.
 A. Ali et al. / Theriogenology 85 (2016) 1576–1581 1579

Table 2
Hemogram (mean  standard error) in male camels with phimosis (PHI) compared to control.

Blood parameter Control n ¼ 10 PHI-Pc n ¼ 34 PHI-Nc n ¼ 9

White blood cells (109/L) 17.83  1.3a 25.82  1.5b 15.44  1.5a
Neutrophils (109/L) 10.68  1.6a 20.48  1.3b 10.5  1.3a
Lymphocytes (109/L) 5.54  0.7 3.67  0.7 3.07  0.8
Monocytes (109/L) 0.86  0.3 0.47  0.1 0.57  0.1
Eosinophils (109/L) 0.72  0.7 1.2  0.4 1.3  0.5
Basophils (109/L) 0.03  0.01 0.002  0.01 0.001  0.01
Red blood cells (1012/L) 10.75  0.6 11.01  0.6 10.01  0.7
Hemoglobin (g/L) 15.03  0.7 15.26  0.7 14.2  0.6
Hematocrit (%) 28.01  1.5 29  1.4 28  1.4
Mean corpuscular volume (fl) 26.2  0.5 26.41  0.4 26.11  0.4
Mean corpuscular hemoglobin (pg) 14.11  0.5 13.97  0.4 13.32  0.5
Mean corpuscular hemoglobin concentration (g/dL) 53.86  1.9 53.23  1.7 53.28  1.8
Platelet count (109/L) 469.21  214 458.72  245 458.72  245
a,b
Values in the same row with different superscript letters differ significantly (P < 0.05).
c
PHI-P, phimosis with detectable pathologic lesions; PHI-N, phimosis with no detectable pathologic lesions.

Preputial squamous cell carcinoma (SCC) was diagnosed
in one camel with PHI. The tip of the prepuce showed
edema, inflammation, and ulceration. Histopathology
revealed the presence of the characteristic nests with var-
iable degrees of keratinization (keratin pearl). The
neoplastic cells were pleomorphic and rounded in shape
with rare mitotic features (Fig. 1D–F).
Penile fat necrosis was observed in another case with
PHI. A firm structure with dimensions of 7.4  4.2 cm was
observed on the dorsum of the glans penis. Two holes filled

Fig. 2. Nitric oxide metabolites and testosterone concentrations (means  standard error) in the sera of male dromedary camels diagnosed with phimosis
compared to control. (PHI-P, phimosis with detectable pathologic lesions; PHI-N, phimosis with no pathologic lesions). abValues with different letter(s) differ
significantly (P ¼ 0.002).
1580 A. Ali et al. / Theriogenology 85 (2016) 1576–1581
with waxy material were noticed in the center of this mass.
Examination of Hematoxylin and Eosin-stained sections
revealed that the necrotic fat cells had lost their cellular
outline, and the cytoplasm had become an amorphous
mass of necrotic material (Fig. 1G–I).
The group with detectable pathologic lesions (PHI-P)
had significantly greater white blood cell (P ¼ 0.001) and
neutrophil (P ¼ 0.0001) counts than those without lesions
(PHI-N) or the control group (Table 2).
The group with noticeable pathologic lesions (PHI-P)
showed significantly (P ¼ 0.002) higher serum NOM con-
centrations than those without detectable lesions (PHI-N)
or the control group (Fig. 2).
No significant difference was detected among groups
with regard to the serum testosterone concentration
(Fig. 2).
4. Discussion
Among the animals in this study, most cases of PHI were
associated with lesions of the prepuce or penis. The
behavior of the male dromedary changes dramatically
during the rutting season, and he becomes vicious in his
keenness to compete with other males for a larger numbers
of females in estrus. Consequently, biting, nudging, strug-
gling, and fighting can result in serious damage to the
copulatory organs as the vulnerable sites of the contenders.
Infectious agents, however, should not be overlooked. The
elevated leukocyte count, mainly because of neutrophilia,
may support this opinion. In addition, injuries from solid
objects, bad management, contact with physical or chem-
ical irritants, and heavy tick infestation have been involved
directly or indirectly in the pathologies of the copulatory
organs in the male dromedary [14]. It is worth mentioning
that some infertile female camels are treated with tradi-
tional folk remedies placed in their copulatory organs.
These preparations may be irritating and cause blistering
and inflammatory changes to the free portion of the penis
upon contact with them during the act of coitus. Unsur-
prisingly, there was a relatively higher incidence of penile
lacerations in the cases with PHI. Trauma because of bites
from other males (Supplementary File) is the most com-
mon complaint in the male dromedary [14,15]. Sand
masturbation, which has been reported in male camels
[16], might also be a predisposing factor for penile and
preputial pathologies.
Fat necrosis is a form of necrosis characterized by the
action of digestive enzymes on fat [17,18]. The enzyme
lipase releases fatty acids from triglycerides, and then, the
fatty acids combine with calcium to form soaps, which
appear as white chalky deposits [17]. This condition is
usually associated with trauma [19]. The site and the large
size of the fat necrosis lesion observed in this study was
enough to prevent penis extension. After surgical removal
of this outgrowth, the animal no longer suffered from PHI.
Cutaneous SCCs are malignant epidermal neoplasms
occurring in humans and animals [17,20,21]. Cases of SCC
of the penis and prepuce have been confirmed in horses,
dogs, and bulls [17,22]. It is the most common penile and
preputial neoplasm in the horse and is mainly found in
older stallions [21,23]. However, in this study, SCC was
observed in a young male dromedary. Squamous cell car-
cinomas can cause discomfort and lead to serious com-
plications [23]. Castration, coat color, poor hygiene, and
various infectious agents have all been suggested as pre-
disposing factors for the development of this type of
tumor in horses [21]. The narrowing and tenderness of the
preputial orifice because of edema and ulceration were the
probable reasons for the inability to extend the penis in
the investigated male.
Nitric oxide metabolites were high in the male drome-
daries with detectable pathologic lesions in their repro-
ductive organs. Under normal physiological conditions,
nitric oxide (NO) provides an anti-inflammatory effect by
preventing the adhesion and release of oxidants by acti-
vated neutrophils in the microvasculature; however, in
abnormal situations, NO is considered as a proin-
flammatory mediator that induces inflammation because
of over-production [24–26]. In accordance with the present
data, NO has been involved in the pathogenesis of inflam-
matory disorders of the joint, gut, and lungs [26]. Proin-
flammatory effects include vasodilation, edema,
cytotoxicity, and the mediation of cytokine-dependent
processes that can lead to tissue destruction [27]. There-
fore, NO inhibitors represent an important therapeutic
advance in the management of inflammatory diseases [26].
Collectively, NO exerts multiple modulating effects on
inflammation. Low concentrations of NO, produced by
constitutive and neuronal nitric oxide synthases, inhibit
adhesion molecule expression, cytokine and chemokine
synthesis, and leukocyte adhesion and transmigration.
However, in higher concentrations, NO can be proin-
flammatory and toxic to tissues [25].
Testosterone concentrations did not differ between the
PHI and control male dromedaries. Preliminary animal and
human studies have suggested that testosterone may
facilitate erection by acting as a vasodilator of the penile
arterioles and cavernous sinusoids [7,28]. Researchers have
theorized that testosterone increases the expression of ni-
tric oxide synthase and phosphodiesterase type 5, both
principal enzymes involved in the erectile process [7,28].
However, a review of the relevant literature from 1939 to
2005 has led to a general conclusion that there is a lack of
association between serum testosterone concentrations,
when present in normal or moderately low concentrations,
and erectile function [29]. In human patients, erectile
function is more likely to improve with testosterone ther-
apy only in patients with severe degrees of hypogonadism
[29].
In summary, the PHI in the dromedary camels was
mainly associated with preputial and penile pathologies,
which may be attributed to trauma and inflammation. The
presence of pathologic lesions in the cases of PHI was
associated with leukocytosis, neutrophilia, and high NOM
concentrations.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.theriogenology.2016.01.011.
 A. Ali et al. / Theriogenology 85 (2016) 1576–1581
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