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Morphological Studies on the Third Eyelid and its Related Structures in the One-Humped Camel (Camelus dromedarius)

Authors:
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
71
The third eyelid of the one- humped camel Al-Ramadan and Ali
Fig (10): A photograph showing a dorsolateral view of the hyoid apparatus
of the rabbit.
1- Basihyoideum (Corpus).
2- Thyroh yoideum (Cornu majus).
3- Ceratohyoideum (Cornu
minus).
4- Processua lingualis.
Morphological Studies on the Third Eyelid and its
Related Structures in the One-Humped Camel
(Camelus dromedarius)
Saeed Y. Al-Ramadan*, Abdelhadi M. Ali
Department of Anatomy, College of Veterinary Medicine and Animal Resources, King
Faisal University
________________________________________________________________
With 8 figures Received December 2011, accepted for publication January 2012
Abstract
The objective of the study was to
characterize the macro- and micro-
scopic features of the third eyelid,
also called the nictitating mem-
brane, and associated structures in
the one-humped camel. The texture,
length, thickness, and width of the
normal third eyelid were studied in
adult camels of both sexes. The re-
sults showed that the third eyelid of
the camel was formed of a relatively
large semilunar fold of conjunctiva
that extended up to 3 cm from the
medial canthus of the eye, over the
anterior surface of the globe. Histo-
logical examination revealed that
the third eyelid of the camel was
formed of glandular and lymphoid
tissues that were enveloped by fi-
brous connective tissue and sup-
ported by a cartilaginous plate. Both
the bulbar and palpebral surfaces of
the third eyelid were covered with
stratified squamous nonkeratinized
epithelium. Many goblet cells were
interspersed among the epithelial
cells that covered the bulbar sur-
face, especially near the base of the
third eyelid. The stroma underneath
the epithelium was composed of
fibrous connective tissue that was
infiltrated with different types of leu-
kocytes and that surrounded glan-
dular tissue and lymphoid nodules.
The cartilage that supported the
third eyelid was of the elastic type
and formed of two parts. A T-
shaped segment of cartilage existed
within the membrane of the third
eyelid and a root-shaped appendix
was embedded within the gland of
the third eyelid. The gland of the
third eyelid was also examined and
it was found to be a tubuloalveolar
mucous gland.
Key words
Third eyelid, nictitating membrane,
lacrimal gland, camel, microscopy
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
72
The third eyelid of the one- humped camel Al-Ramadan and Ali
Introduction
The camel inhabits arid and semi-
arid areas and its eyes are im-
portant for its survival. In studies of
the adaptability of the camel, it is
necessary to define the structural
features of the third eyelid, the nicti-
tating membrane, which is a promi-
nent semilunar fold of the conjuncti-
va that is situated at the medial an-
gle of the eye. The third eyelid is
important for the production and dis-
tribution of tears, the removal of oc-
ular debris, and the protection of the
eye, and has significant immunolog-
ic functions (Schlegel et al., 2003).
Movement of the third eyelid is pas-
sive, owing to the absence of mus-
cles that could move the eyelid ac-
tively. The location of the free mar-
gin of the third eyelid is controlled
by the position of the eyeball.
Several studies have been conduct-
ed on the eye of the camel and its
related structures (Abou-Elmagd
1992; Wang 2002; Kumar et al
2003; Mohammadpour 2009). How-
ever, to the authors’ knowledge, no
detailed study has been performed
on the structure of the third eyelid.
Thus, the aim of the present study
was to investigate the morphological
and histological features of the third
eyelid and its associated structures
in the one-humped camel. The find-
ings will enrich the comparative
anatomy of domestic animals, pro-
vide a basis for further research on
the adaptability of this animal to the
desert environment, and might have
clinical applications.
Materials and Methods
Morphological examinations of the
third eyelid were conducted on ten
clinically healthy adult camels of
both sexes at the Al-Omran Slaugh-
ter House, Al-Ahsa, Saudi Arabia.
The macroscopic preparations were
performed using a magnifying lens.
The samples were bathed in 60
80% alcohol and 0.54% acetic acid
solution to increase the visibility of
the anatomical elements. For the
histological examination, the whole
eyeball with its accessory structures
was collected from each camel im-
mediately after slaughter. The mate-
rials collected were fixed in 4%
buffered formaldehyde solution,
washed in running water for 24 h,
dehydrated in a graded series of
alcohol (70100% alcohol for 18 h),
embedded in paraffin, and cut into
longitudinal sections that were 5-µm
thick with a Leica RM 2045 micro-
tome (Microsystem GmbH, Wetzler,
Germany). The sections were
stained with hematoxylin eosin
(H&E), Orcein, and Masson tri-
chrome. The sections were evaluat-
ed using a light microscope at mag-
nifications of 5×, 10×, 40×, and
100×. Histological images were ob-
tained with an Olympus BX 41 mi-
croscope and Olympus DP-12 digi-
tal camera (Olympus Corp., Tokyo,
Japan).
For macroscopic investigation of the
cartilage of the third eyelid, a modi-
fication of the maceration technique
described by Schlegel et al. (2001)
was used. Briefly, the third eyelid
was macerated carefully in an
aqueous solution of 2% sodium
base for a maximum of 18 h at
40°C, which was observed periodi-
cally. After maceration, the samples
were washed three times in phos-
phate buffered saline (pH 6.8) and
conserved subsequently in 0.15%
formalin. All samples were photo-
graphed with a Sony α-550 camera
(Sony Corp., Pathumthani, Thai-
land).
Results
The third eyelid of the camel was
formed of a relatively large semilu-
nar fold of conjunctiva that extended
up to 3 cm from the medial canthus
of the eye, into the anterior surface
of the globe. The marginal part of
the third eyelid was thin and pig-
mented (Fig. 1). Both the bulbar and
palpebral surfaces were covered
with stratified squamous nonkeratin-
ized epithelium (Fig. 2). Many goblet
cells were interspersed among the
epithelial cells that covered the
bulbar surface, especially near the
base of the third eyelid (Fig. 3). The
stroma beneath the epithelium was
formed of fibrous connective tissue
which was infiltrated with different
types of leukocyte and surrounded
the glandular tissue and lymphoid
nodules (Figs 3, 4 and 5). In all the
specimens examined, no muscle
fibers were detected within the third
eyelid.
The third eyelid of the camel was
supported by a cartilage. The carti-
lage was dissected carefully and
found to be composed of two parts:
a T-shaped segment within the
membrane of the third eyelid and a
root-shaped appendix embedded
within the gland of the third eyelid.
The T-shaped segment comprised a
cross-bar that was parallel to the
free margin of the third eyelid and a
long narrow shaft that continued
caudally as the root-shaped part,
which was embedded in the gland
of the third eyelid (Fig. 6). Orcein
staining revealed that the cartilage
was of the elastic type (Fig. 4).
Macroscopically, the gland of the
third eyelid was oval in shape with a
convex palpebral surface and a
concave bulbar surface (Fig. 7). Mi-
croscopically, the gland was found
to be a tubuloalveolar in type and
mucous in nature (Fig. 8). Two
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
73
The third eyelid of the one- humped camel Al-Ramadan and Ali
Introduction
The camel inhabits arid and semi-
arid areas and its eyes are im-
portant for its survival. In studies of
the adaptability of the camel, it is
necessary to define the structural
features of the third eyelid, the nicti-
tating membrane, which is a promi-
nent semilunar fold of the conjuncti-
va that is situated at the medial an-
gle of the eye. The third eyelid is
important for the production and dis-
tribution of tears, the removal of oc-
ular debris, and the protection of the
eye, and has significant immunolog-
ic functions (Schlegel et al., 2003).
Movement of the third eyelid is pas-
sive, owing to the absence of mus-
cles that could move the eyelid ac-
tively. The location of the free mar-
gin of the third eyelid is controlled
by the position of the eyeball.
Several studies have been conduct-
ed on the eye of the camel and its
related structures (Abou-Elmagd
1992; Wang 2002; Kumar et al
2003; Mohammadpour 2009). How-
ever, to the authors’ knowledge, no
detailed study has been performed
on the structure of the third eyelid.
Thus, the aim of the present study
was to investigate the morphological
and histological features of the third
eyelid and its associated structures
in the one-humped camel. The find-
ings will enrich the comparative
anatomy of domestic animals, pro-
vide a basis for further research on
the adaptability of this animal to the
desert environment, and might have
clinical applications.
Materials and Methods
Morphological examinations of the
third eyelid were conducted on ten
clinically healthy adult camels of
both sexes at the Al-Omran Slaugh-
ter House, Al-Ahsa, Saudi Arabia.
The macroscopic preparations were
performed using a magnifying lens.
The samples were bathed in 60
80% alcohol and 0.54% acetic acid
solution to increase the visibility of
the anatomical elements. For the
histological examination, the whole
eyeball with its accessory structures
was collected from each camel im-
mediately after slaughter. The mate-
rials collected were fixed in 4%
buffered formaldehyde solution,
washed in running water for 24 h,
dehydrated in a graded series of
alcohol (70100% alcohol for 18 h),
embedded in paraffin, and cut into
longitudinal sections that were 5-µm
thick with a Leica RM 2045 micro-
tome (Microsystem GmbH, Wetzler,
Germany). The sections were
stained with hematoxylin eosin
(H&E), Orcein, and Masson tri-
chrome. The sections were evaluat-
ed using a light microscope at mag-
nifications of 5×, 10×, 40×, and
100×. Histological images were ob-
tained with an Olympus BX 41 mi-
croscope and Olympus DP-12 digi-
tal camera (Olympus Corp., Tokyo,
Japan).
For macroscopic investigation of the
cartilage of the third eyelid, a modi-
fication of the maceration technique
described by Schlegel et al. (2001)
was used. Briefly, the third eyelid
was macerated carefully in an
aqueous solution of 2% sodium
base for a maximum of 18 h at
40°C, which was observed periodi-
cally. After maceration, the samples
were washed three times in phos-
phate buffered saline (pH 6.8) and
conserved subsequently in 0.15%
formalin. All samples were photo-
graphed with a Sony α-550 camera
(Sony Corp., Pathumthani, Thai-
land).
Results
The third eyelid of the camel was
formed of a relatively large semilu-
nar fold of conjunctiva that extended
up to 3 cm from the medial canthus
of the eye, into the anterior surface
of the globe. The marginal part of
the third eyelid was thin and pig-
mented (Fig. 1). Both the bulbar and
palpebral surfaces were covered
with stratified squamous nonkeratin-
ized epithelium (Fig. 2). Many goblet
cells were interspersed among the
epithelial cells that covered the
bulbar surface, especially near the
base of the third eyelid (Fig. 3). The
stroma beneath the epithelium was
formed of fibrous connective tissue
which was infiltrated with different
types of leukocyte and surrounded
the glandular tissue and lymphoid
nodules (Figs 3, 4 and 5). In all the
specimens examined, no muscle
fibers were detected within the third
eyelid.
The third eyelid of the camel was
supported by a cartilage. The carti-
lage was dissected carefully and
found to be composed of two parts:
a T-shaped segment within the
membrane of the third eyelid and a
root-shaped appendix embedded
within the gland of the third eyelid.
The T-shaped segment comprised a
cross-bar that was parallel to the
free margin of the third eyelid and a
long narrow shaft that continued
caudally as the root-shaped part,
which was embedded in the gland
of the third eyelid (Fig. 6). Orcein
staining revealed that the cartilage
was of the elastic type (Fig. 4).
Macroscopically, the gland of the
third eyelid was oval in shape with a
convex palpebral surface and a
concave bulbar surface (Fig. 7). Mi-
croscopically, the gland was found
to be a tubuloalveolar in type and
mucous in nature (Fig. 8). Two
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
74
The third eyelid of the one- humped camel Al-Ramadan and Ali
types of secretory units could be
defined: acini with a small lumen,
which were lined with tall pyramidal
cells, and tubules with a large lu-
men, which were lined with cuboidal
epithelial cells. Elongated nuclei
were observed frequently around
the acini. Intralobular ducts could
also be detected, lined with cuboidal
to short columnar cells with large
lumens (Fig. 8).
Discussion
The results of this study revealed
that the third eyelid of the adult one-
humped camel was formed of a rel-
atively large semilunar fold of con-
junctiva that extended up to 3 cm
from the medial canthus of the eye,
over the anterior surface of the
globe. Movement of the third eyelid
is achieved by the forces which are
generated when the animal shuts its
upper and lower eyelids (Getty,
1975 in domestic animals; Umeda
et al., 2010 in canines). Several pro-
tective functions that are important
for the globe of the eye have been
attributed to the third eyelid, such as
the production and spread of tears,
removal of foreign materials, and
immunological activity involving the
secretion of immunoglobulins (Klec-
kowska-Nawrot and Dziegiel, 2007;
2008 in the pig; Alexandre-Pires et
al, 2008 in the dog; Moham-
madpour, 2009 in the camel; Bay-
raktaroğlu and Ergün, 2010 in the
Angora rabbit). These functions
seem to be particularly important for
animals that live in the desert,
where sand storms are very com-
mon. Such animals need the extra
protection for the eyes that is pro-
vided by a well-developed third eye-
lid.
The present study revealed the
presence of many goblet cells at the
bulbar surface of the third eyelid. In
dogs, removal of the third eyelid
leads to qualitative changes in the
tears, including reduction of the ba-
sal tear volume and an increase in
pH. In addition, a decrease in the
layers of superficial cells and de-
tachment of hemidesmosomes in
the basal cell layers of the cornea
have been reported (Saito et al.,
2004). These findings suggest that
the nictitating membrane might play
a more important role than was pre-
viously thought in protecting the oc-
ular surface, because the mucin
produced by the goblet cells might
affect the stability of the tear film
(Saito et al., 2004; Umeda et al,
2010).
Morphologic observation of the
specimens in the present study re-
vealed that the cartilage of the third
eyelid in the camel had two parts: a
T-shaped segment within the mem-
brane of the third eyelid and a root-
shaped part embedded within the
gland of the third eyelid. The T-
shaped segment comprised a cross-
bar that lay parallel to the free mar-
gin of the third eyelid and a long
narrow shaft that continued caudally
as the root-shaped appendix, which
was rooted within the gland. In all
domestic mammals studied, the
third eyelid is supported by a carti-
lage, which shows various shapes
and forms (Getty, 1975). In pigs and
cattle, it has a typical anchor form.
In the dog, it has a prominent ap-
pendix, which is cone-shaped at the
basal end and then extends in a
slightly curved form, becomes con-
tinually broader, and finally forms a
triangular plate with a crescent-like
crossbar. In contrast, the cartilage
of the third eyelid of the cat has a
paddle-shaped proximal part that
becomes thinner over a short dis-
tance and extends to a triangular
plate in the distal direction; the
cross-bar has a reverse S-form. The
cartilage of small ruminants begins
as a thin rod, extends in a distal di-
rection in a slightly curved form, and
ends in an oval plate, whereas its
cross-bar has a crescent-like shape
(Schlegel et al., 2001).
Histological examination of the carti-
lage of the third eyelid of the camel
showed it to be of the elastic type.
This is contrary to Mohammadpour,
2009 who described it to be formed
of hyaline cartilage. The finding of
the elastic cartilage in the camel is
not an exceptional one. A similar
type of cartilage has been reported
in the third eyelid of the cat and
horse, whereas hyaline cartilage
has been reported in dogs, cattle,
and small ruminants (Bank, 1993,
Schlegel et al., 2001).
The current study showed that the
gland of the third eyelid of the camel
was oval in shape with a convex
palpebral surface and a concave
bulbar surface, and was found to be
a tubuloalveolar serous gland. Simi-
lar data have been reported previ-
ously for the camel (Kumar et al.,
2003; Mohammadpour, 2009). In
accordance with previous studies
conducted on the Harderian glands
of camels (Abou-Elmagd, 1992;
Kumar et al., 2003), an intralobular
duct lined with a single layer of cu-
boidal to low columnar epithelium
was observed between the glandu-
lar acini. Similar findings have also
been reported in other mammals
(Sakai and Yohro, 1981; Gargiulo et
al., 1999; Pinard et al., 2003;
Munkeby et al., 2006; Rehorek and
Smith, 2006). However, in some de-
sert rodents, only tubular units have
been reported (Djeridane, 1992).
The elongated nuclei around the
acini might represent the nuclei of
myoepithelial cells. Electron micros-
copy has revealed the presence of
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
75
The third eyelid of the one- humped camel Al-Ramadan and Ali
types of secretory units could be
defined: acini with a small lumen,
which were lined with tall pyramidal
cells, and tubules with a large lu-
men, which were lined with cuboidal
epithelial cells. Elongated nuclei
were observed frequently around
the acini. Intralobular ducts could
also be detected, lined with cuboidal
to short columnar cells with large
lumens (Fig. 8).
Discussion
The results of this study revealed
that the third eyelid of the adult one-
humped camel was formed of a rel-
atively large semilunar fold of con-
junctiva that extended up to 3 cm
from the medial canthus of the eye,
over the anterior surface of the
globe. Movement of the third eyelid
is achieved by the forces which are
generated when the animal shuts its
upper and lower eyelids (Getty,
1975 in domestic animals; Umeda
et al., 2010 in canines). Several pro-
tective functions that are important
for the globe of the eye have been
attributed to the third eyelid, such as
the production and spread of tears,
removal of foreign materials, and
immunological activity involving the
secretion of immunoglobulins (Klec-
kowska-Nawrot and Dziegiel, 2007;
2008 in the pig; Alexandre-Pires et
al, 2008 in the dog; Moham-
madpour, 2009 in the camel; Bay-
raktaroğlu and Ergün, 2010 in the
Angora rabbit). These functions
seem to be particularly important for
animals that live in the desert,
where sand storms are very com-
mon. Such animals need the extra
protection for the eyes that is pro-
vided by a well-developed third eye-
lid.
The present study revealed the
presence of many goblet cells at the
bulbar surface of the third eyelid. In
dogs, removal of the third eyelid
leads to qualitative changes in the
tears, including reduction of the ba-
sal tear volume and an increase in
pH. In addition, a decrease in the
layers of superficial cells and de-
tachment of hemidesmosomes in
the basal cell layers of the cornea
have been reported (Saito et al.,
2004). These findings suggest that
the nictitating membrane might play
a more important role than was pre-
viously thought in protecting the oc-
ular surface, because the mucin
produced by the goblet cells might
affect the stability of the tear film
(Saito et al., 2004; Umeda et al,
2010).
Morphologic observation of the
specimens in the present study re-
vealed that the cartilage of the third
eyelid in the camel had two parts: a
T-shaped segment within the mem-
brane of the third eyelid and a root-
shaped part embedded within the
gland of the third eyelid. The T-
shaped segment comprised a cross-
bar that lay parallel to the free mar-
gin of the third eyelid and a long
narrow shaft that continued caudally
as the root-shaped appendix, which
was rooted within the gland. In all
domestic mammals studied, the
third eyelid is supported by a carti-
lage, which shows various shapes
and forms (Getty, 1975). In pigs and
cattle, it has a typical anchor form.
In the dog, it has a prominent ap-
pendix, which is cone-shaped at the
basal end and then extends in a
slightly curved form, becomes con-
tinually broader, and finally forms a
triangular plate with a crescent-like
crossbar. In contrast, the cartilage
of the third eyelid of the cat has a
paddle-shaped proximal part that
becomes thinner over a short dis-
tance and extends to a triangular
plate in the distal direction; the
cross-bar has a reverse S-form. The
cartilage of small ruminants begins
as a thin rod, extends in a distal di-
rection in a slightly curved form, and
ends in an oval plate, whereas its
cross-bar has a crescent-like shape
(Schlegel et al., 2001).
Histological examination of the carti-
lage of the third eyelid of the camel
showed it to be of the elastic type.
This is contrary to Mohammadpour,
2009 who described it to be formed
of hyaline cartilage. The finding of
the elastic cartilage in the camel is
not an exceptional one. A similar
type of cartilage has been reported
in the third eyelid of the cat and
horse, whereas hyaline cartilage
has been reported in dogs, cattle,
and small ruminants (Bank, 1993,
Schlegel et al., 2001).
The current study showed that the
gland of the third eyelid of the camel
was oval in shape with a convex
palpebral surface and a concave
bulbar surface, and was found to be
a tubuloalveolar serous gland. Simi-
lar data have been reported previ-
ously for the camel (Kumar et al.,
2003; Mohammadpour, 2009). In
accordance with previous studies
conducted on the Harderian glands
of camels (Abou-Elmagd, 1992;
Kumar et al., 2003), an intralobular
duct lined with a single layer of cu-
boidal to low columnar epithelium
was observed between the glandu-
lar acini. Similar findings have also
been reported in other mammals
(Sakai and Yohro, 1981; Gargiulo et
al., 1999; Pinard et al., 2003;
Munkeby et al., 2006; Rehorek and
Smith, 2006). However, in some de-
sert rodents, only tubular units have
been reported (Djeridane, 1992).
The elongated nuclei around the
acini might represent the nuclei of
myoepithelial cells. Electron micros-
copy has revealed the presence of
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
76
The third eyelid of the one- humped camel Al-Ramadan and Ali
myoepithelial cells between the lin-
ing glandular cells and the basal
lamina in the Harderian gland of the
camel (Abou-Elmagd, 1992; Kumar
et al., 2003) and the rabbit (Bay-
raktaroglu and Ergun 2010).
Acknowledgements
This work was supported by the
Scientific Research Deanship, King
Faisal University (Grant No. 10136).
Our thanks to the staff at Al-Omran
Slaughter House, Alahsa, Saudi
Arabia.
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Amselgruber, (2003): IgA
and secretory component
(SC) in the third eyelid of
domestic animals: A com-
parative study. Vet Oph-
thalmol. 6, 157161.
Umeda, Y., S. Nakamura, K. Fujiki ,
H. Toshida, A. Saito, and A.
Murakami (2010): Distribu-
tion of goblet cells and
MUC5AC mRNA in the ca-
nine nictitating membrane.
Exp. Eye Res. 91, 721-726.
Wang, J., (2002): The arterial sup
ply to the eye of the Bactrian
camel (Camelus bactrianus).
Vet. Res. Commun. 26, 505-
512.
______________
Corresponding author:
Tel.: 966 358 16600; Fax: 966 358
16635; e-mail: salramadan@kfu.edu.sa
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
77
The third eyelid of the one- humped camel Al-Ramadan and Ali
myoepithelial cells between the lin-
ing glandular cells and the basal
lamina in the Harderian gland of the
camel (Abou-Elmagd, 1992; Kumar
et al., 2003) and the rabbit (Bay-
raktaroglu and Ergun 2010).
Acknowledgements
This work was supported by the
Scientific Research Deanship, King
Faisal University (Grant No. 10136).
Our thanks to the staff at Al-Omran
Slaughter House, Alahsa, Saudi
Arabia.
References
Abou-Elmagd, A. (1992): Ultrastruc
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Trindade, (2008): Immuno-
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nary histology. Mosbi Inc. St.
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Angora rabbit. Anat. Histol.
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Kleckowska-Nawrot, J., and
Dziegiel P., (2007): Mor-
phology of the third eyelid
and superficial gland of the
third eyelid on pig fetuses.
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428-432.
Kleckowska-Nawrot, J., and
Dziegiel P., (2008): Mor-
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the Third Eyelid in Pig Foe-
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37, 36-40.
Kumar, P., R. K. Jain, and A. N.
Gupta (2003): Histoarchitec-
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camel (Camelus dromedar-
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73, 972-975.
Mohammadpour, A. A., (2009):
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: Magnetic resonance imag-
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Pinard, C. L., M. L. Weiss, A. H.
Brightman, B. W. Fenwick,
and H. J. Davidson, (2003):
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American bison and cattle.
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257-262.
Rehorek, S. J., and T. D. Smith,
(2006): The primate Harde-
rian gland: Does it really ex-
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Saito, A., Y. Watanabe, and T. Ko-
tani, (2004): Morphologic
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thalmol. 6, 157161.
Umeda, Y., S. Nakamura, K. Fujiki ,
H. Toshida, A. Saito, and A.
Murakami (2010): Distribu-
tion of goblet cells and
MUC5AC mRNA in the ca-
nine nictitating membrane.
Exp. Eye Res. 91, 721-726.
Wang, J., (2002): The arterial sup
ply to the eye of the Bactrian
camel (Camelus bactrianus).
Vet. Res. Commun. 26, 505-
512.
______________
Corresponding author:
Tel.: 966 358 16600; Fax: 966 358
16635; e-mail: salramadan@kfu.edu.sa
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
78
The third eyelid of the one- humped camel Al-Ramadan and Ali
Fig (1): The third eyelid of the camel extends from the medial canthus of the eye (A).
Note the marginal pigmented portion (B).
Fig (2): Light micrograph of the third eyelid showing the anterior (A) and posterior (B)
surfaces, with the connective tissue stroma (C) and the cartilage (D) (H&E, X40).
Fig (3): Light micrograph showing the posterior surface of the third eyelid near its base.
Note the goblet cells (A) within the stratified squamous epithelial layer. The stroma of
fibrous connective tissue is infiltrated with different types of leukocyte (B) (Trichrome,
X400).
Fig (4): Light micrograph of the third eyelid of the camel. Note the glandular compo-
nents of the gland of the third eyelid (A) and the cartilage bar (B) that is rooted deeply in
the gland (Orcein, 40×). Insert: higher magnification of (B); note the condensation of the
elastic fibers (X400).
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
79
The third eyelid of the one- humped camel Al-Ramadan and Ali
Fig (1): The third eyelid of the camel extends from the medial canthus of the eye (A).
Note the marginal pigmented portion (B).
Fig (2): Light micrograph of the third eyelid showing the anterior (A) and posterior (B)
surfaces, with the connective tissue stroma (C) and the cartilage (D) (H&E, X40).
Fig (3): Light micrograph showing the posterior surface of the third eyelid near its base.
Note the goblet cells (A) within the stratified squamous epithelial layer. The stroma of
fibrous connective tissue is infiltrated with different types of leukocyte (B) (Trichrome,
X400).
Fig (4): Light micrograph of the third eyelid of the camel. Note the glandular compo-
nents of the gland of the third eyelid (A) and the cartilage bar (B) that is rooted deeply in
the gland (Orcein, 40×). Insert: higher magnification of (B); note the condensation of the
elastic fibers (X400).
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
80
The third eyelid of the one- humped camel Al-Ramadan and Ali
Fig (5): Light micrograph showing the lymphatic nodules (arrows) that were detected
near the base of the third eyelid of the camel (H&E, X100).
Fig (6): A photograph showing the cartilage of the third eyelid. Note the T-shaped
segment with its cross-bar (A) and long narrow shaft (B), which continue as a branched
segment (C) within the gland of the third eyelid.
Fig (7): The third eyelid of the camel with its associated structures: (i) bulbar surface, (ii)
palpebral surface. Free margin of the third eyelid (A), gland of the third eyelid (B).
Fig (8): Light micrograph of the gland of the third eyelid of the camel, showing tubu-
loaloveolar units with acini (A) lined by pyramidal cells, and tubules (T) lined with cu-
boidal to low columnar cells surrounding an empty lumen; (D) intralobular ducts (Orcein,
×100). Insert: higher magnification of the field, note the elongated nuclei (arrow heads)
at the base of the acini (X400).
J. Vet. Anat. Vol 5 No 2, (2012) 71 - 81
81
The third eyelid of the one- humped camel Al-Ramadan and Ali
Fig (5): Light micrograph showing the lymphatic nodules (arrows) that were detected
near the base of the third eyelid of the camel (H&E, X100).
Fig (6): A photograph showing the cartilage of the third eyelid. Note the T-shaped
segment with its cross-bar (A) and long narrow shaft (B), which continue as a branched
segment (C) within the gland of the third eyelid.
Fig (7): The third eyelid of the camel with its associated structures: (i) bulbar surface, (ii)
palpebral surface. Free margin of the third eyelid (A), gland of the third eyelid (B).
Fig (8): Light micrograph of the gland of the third eyelid of the camel, showing tubu-
loaloveolar units with acini (A) lined by pyramidal cells, and tubules (T) lined with cu-
boidal to low columnar cells surrounding an empty lumen; (D) intralobular ducts (Orcein,
×100). Insert: higher magnification of the field, note the elongated nuclei (arrow heads)
at the base of the acini (X400).
Immunohistochemical, cellular localization and ex-
pression of inhibin hormone in the buffalo (Buba-
lus bubalis) adenohypophysis at different ages
Attia H.F. 1*, Kandiel M.M. 2, Ismail T.A.3*, Soliman M. M. 4*,
Nassan M. A. 5, Mansour A. A. 6*
Department of Histology and Cytology1,Theriogenology2 and Biochemistry4, Faculty of
Veterinary Medicine, Benha University, Egypt. Department of Physiology3 and Patholo-
gy5, Faculty of Veterinary Medicine, Zagazig University, Egypt. Department of Genetics6,
Faculty of Agriculture, Ain Shams University, Egypt.
*Department of Medical Laboratories and Medical Biotechnology, Faculty of Applied
Medical sciences, Taif University, Turabuha branch, KSA.
_______________________________________________________________________
With 7 plates, 1 table Received April, accepted for publication August 2012
Abstract
The pituitary adenohypophysis was
obtained from thirty buffaloes-cows,
their age's ranges from one month
to12 years. Sections of adenohy-
pophysis tissues were immuno-
stained for α, βa, and βb subunits of
inhibin hormone. Positive immuno-
staining specific for the α subunits of
inhibin were detected in the cells of
the follicles of the adenohypophysis
in all ages. Moreover, immunostain-
ing specific for the inhibin βa subu-
nits were strong positive at one
month, weak positive at 4.5, 8 and
12 years and were negative at 8
months and 1.5 years. However, the
immunostaining specific for the in-
hibin βb subunits were positive at
one and 8 months, 8 and 12 years
and weak positive at 4.5 years and
negative at 1.5 year. RT-PCR anal-
ysis revealed that both α and βb
subunits are expressed in all ages
except at 1.5 years old animals
while βa subunit is only expressed
at young age.
Key words
Inhibin, buffalo-cows, Adenohypo-
physis, RT-PCR, Immunohisto-
chemistry.
Introduction
There is worldwide interest in buffa-
lo as an animal for meeting the
growing demands of meat and milk
in developing countries. One of the
major breeding problems in buffalos
is its low reproductive efficiency.
Ovarian cyclicity is regulated by hy-
pothalamic hormones, gonadotro-
Animal species in this issue
One-humped camel (Camelus dromedarius)
Kingdom: Animalia, Phylum: Chordata, Class: Mammalia, Oder: Artiodactyla. Family: Camelidae,
Genus: Camelus
Camel is an even-toed ungulate within the genus Camelus, bearing distinctive fatty
deposits known as humps on its back. There are two species of camels: the dromedary
or Arabian camel has a single hump, and the Bactrian camel has two humps. They are
native to the dry desert areas of West Asia, and Central and East Asia, respectively.
Both species are domesticated to provide milk and meat, and as beasts of burden.
The average life expectancy of a camel is 40 to 50 years. A fully grown adult camel
stands 1.85 m at the shoulder and 2.15 m at the hump. The hump rises about 30 inches
(76.20 cm) out of its body. Camels can run at up to 65 km/h (40 mph) in short bursts and
sustain speeds of up to 40 km/h (25 mph).
Fossil evidence indicates that the ancestors of modern camels evolved in North America
during the Palaeogene period, and later spread to most parts of Asia. Humans first
domesticated camels before 2000 BC.
Camels are able to withstand changes in body temperature and water content that
would kill most other animals. Their temperature ranges from 34 °C at night and up to
41 °C during the day, and only above this threshold will they begin to sweat.
(Source: Wikipedia)
... A similar structure was described by BISARIA and BISARIA (1978), KEMPSTER et al. (2002), KLEAEKOWSKA-NAWROT (2005), KLEAEKOWSKA-NAWROT et al. (2015a), KLEAE- KOWSKA-NAWROT et al. (2015b), NICKEL et al. (2004), and SCHLEGEL et al. (2001 in the pig, dog, koala, rat, and domestic ruminants, respectively. However, in the one-humped camel, cat and horse the TE cartilage was composed of elastic tissue (AL- RAMADAN & ALI 2012;CONSTANTINESCU & MOORE 1998;and SCHLEGEL et al. 2001). The conjunctival and ocular surface of the TE in the red kangaroo, similarly to the dog and wild ruminants, consisted of non-keratinized stratified squamous epithelium with numerous goblet cells (AL-RAMADAN & ALI 2012;CAZACU 2010;KLEAEKOWSKA-NAWROT et al. 2015a;KLEAEKOW-SKA-NAWROT et al. 2015b). ...
... However, in the one-humped camel, cat and horse the TE cartilage was composed of elastic tissue (AL- RAMADAN & ALI 2012;CONSTANTINESCU & MOORE 1998;and SCHLEGEL et al. 2001). The conjunctival and ocular surface of the TE in the red kangaroo, similarly to the dog and wild ruminants, consisted of non-keratinized stratified squamous epithelium with numerous goblet cells (AL-RAMADAN & ALI 2012;CAZACU 2010;KLEAEKOWSKA-NAWROT et al. 2015a;KLEAEKOW-SKA-NAWROT et al. 2015b). ...
... The SGTE of the red kangaroo was located between the medial straight and ventral straight muscle and was partially covered by the ventral oblique muscle of the eye. A similar location of this gland was demonstrated in other mammal species (AL- RAMADAN & ALI 2012;CAZACU 2010;CONSTANTINESCU & MCCLURE 1990;KLEAEKOW-SKA-NAWROT & DZIÊGIEL 2007;KEMPSTER et al. 2002;KLEAEKOWSKA-NAWROT et al. 2013;KLEAE-KOWSKA-NAWROT et al. 2015a;MOHAMMADPOUR 2009;NUYTTENS & SIMOENS 1995;PINARD et al. 2003;SCHLEGEL et al. 2001). Similarly to the LG, the SGTE was uniform and undivided. ...
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A study concerning the upper (UE) and lower (LE) eyelids, lacrimal gland (LG), superficial gland of the third eyelid (SGTE) and third eyelid (TE) was conducted on 4 sexually mature red kangaroos (2 males and 2 females). Gross anatomical, histological, histometrical, histochemical and ultrastructural (TEM) components were compared. Tissue sections were stained with haematoxylin and eosin, azan-trichrome, van Gieson, Masson-Goldner trichrome, methyl green-pyronin Y, periodic acid-Schiff, alcian blue pH 2.5, aldehyde fuchsin and Hale's dialysed iron. The location of the LG, SGTE, TE, UE and LE was similar to that of other mammals. Organized lymphoid follicles were also found in the LE. The TE resembled the letter T and was composed of cartilage (hyaline tissue). The LG was relatively larger than the SGTE. The LG and SGTE were multilobar tubuloacinar glands. The LG had more plasma cells than the SGTE. The SGTE and LG secretions were mucoserous in composition. The TEM study showed that the secretory cells of the LG and SGTE have a similar ultrastructural appearance. Two types of secretory vesicles were detected in the cytoplasm in acini and one type of secretory vesicle was found in the tubules of these glands. © Institute of Systematics and Evolution of Animals, PAS, Kraków, 2016.
... LG contains a high concentration of lysozyme, which can digest bacterial cells walls, and a gamma globulin protein fraction which also contributes to the antibacterial property of tears [39]. The LG plays an important role in the protection of the cornea and the conjunctiva from drying up and also nourishes and lubricates the eye, contributes in metabolite exchange, protects the cornea surface from injuries caused by foreign bodies, and has bactericidal and bacteriostatic properties [3,4,30,48,49]. According to Dartt [7], the tear film consists of water, electrolytes and proteins. ...
... SGTE has a tubulo-acinar structure and produces a secretion of mucoalbuminous character [9,19,40]. SGTE encircles a crossbar of third eyelid, where numerous lymph nodules are present on the underside of third eyelid [3,39]. The third eyelid is also described as plicas semilunaris conjuncitve [33,34]. ...
... The role of the third eyelid is mechanical protection of the cornea, as well as local immunological protection by substances which are present in lymphoid nodules and by tear film distribution on the corneal surface [19,25]. The movement of the third eyelid in animals has a passive character, which is connected with the lack of muscles actively moving the eyelid [3]. However in birds, the movement of the third eyelid is active, which is associated with the presence of two eyelid muscles (m. ...
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The lacrimal gland (LG) and superficial gland of the third eyelid (SGTE) belong to accessory organs of the eye. The aim of the present studies was to evaluate the histological, histochemical and fine structure of the LG and SGTE obtained from 3 adult females and 2 adult males of alpaca (Vicugna pacos). The LG was situated in the dorsolateral angle of the orbit between the dorsal rectus and the lateral rectus muscles. The SGTE was located between the medial rectus muscle, the ventral rectus muscle and was partially covered by the ventral oblique muscle of the eyeball. There were no effect of gender on the morphometry of examined LG and SGTE. The third eyelid resembles an anchor in shape. During histological and ultrastructural analyses using light and transmission electron microscopy, it was established that the LG and SGTE are tubulo-acinar glands with mucoserous characters. The LG contains either lymphocytes or plasma cells, while SGTE had rare plasma cells and numerous lymphocytes in connective tissue. The cartilage of the third eyelid was composed of hyaline tissue. Numerous aggregations of lymphocytes as lymph nodules in bulbar surface of the third eyelid were observed. The LG and SGTE secretory cells exhibited a similar ultrastructure appearance in electron microscopic examination, with secretory cells tightly filled with intracytoplasmatic secretory granules and numerous clusters of mucus of different sizes which were observed in the peripheral cells compartment.
... Similar findings were observed in red kangaroos, koalas, pigs, dogs, rats and domestic and wild ruminants (Bisaria & Bisaria, 1978;Kempster et al., 2002;Klećkowska-Nawrot & Dzięgiel, 2007;Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Krasucki, et al. 2015, Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Szara, et al. 2015Nickel et al., 2004;Schlegel et al., 2001;Smollich & Michel, 1992). In the horse, cat, one-humped camel and small Indian mongoose, the cartilage of the third eyelid was composed of elastic tissue (Al-Ramadan & Ali, 2012;Constantinescu & Moore, 1998;Kamali et al., 2015;Schlegel et al., 2001). In the Sulawesi bear cuscus, the palpebral conjunctival surface of the third eyelid was covered by a non-keratinised stratified squamous epithelium with three to six layers of nucleated cells and goblet cells, while the bulbar conjunctival surface contained a stratified columnar epithelium with three to five layers of epithelial cells with numerous goblet cells, which were strongly PAS and Alcian blue pH 2.5 positive. ...
... In the Sulawesi bear cuscus, the palpebral conjunctival surface of the third eyelid was covered by a non-keratinised stratified squamous epithelium with three to six layers of nucleated cells and goblet cells, while the bulbar conjunctival surface contained a stratified columnar epithelium with three to five layers of epithelial cells with numerous goblet cells, which were strongly PAS and Alcian blue pH 2.5 positive. In red kangaroos, dogs and wild ruminants, the bulbar conjunctiva consisted of a non-keratinised stratified squamous epithelium with goblet cells (Al-Ramadan, 2015;Al-Ramadan & Ali, 2012;Cazacu, 2010;Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Krasucki, et al. 2015, Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Szara, et al. 2015). ...
... Similar findings were observed in red kangaroos, koalas, pigs, dogs, rats and domestic and wild ruminants (Bisaria & Bisaria, 1978;Kempster et al., 2002;Klećkowska-Nawrot & Dzięgiel, 2007;Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Krasucki, et al. 2015, Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Szara, et al. 2015Nickel et al., 2004;Schlegel et al., 2001;Smollich & Michel, 1992). In the horse, cat, one-humped camel and small Indian mongoose, the cartilage of the third eyelid was composed of elastic tissue (Al-Ramadan & Ali, 2012;Constantinescu & Moore, 1998;Kamali et al., 2015;Schlegel et al., 2001). In the Sulawesi bear cuscus, the palpebral conjunctival surface of the third eyelid was covered by a non-keratinised stratified squamous epithelium with three to six layers of nucleated cells and goblet cells, while the bulbar conjunctival surface contained a stratified columnar epithelium with three to five layers of epithelial cells with numerous goblet cells, which were strongly PAS and Alcian blue pH 2.5 positive. ...
... In the Sulawesi bear cuscus, the palpebral conjunctival surface of the third eyelid was covered by a non-keratinised stratified squamous epithelium with three to six layers of nucleated cells and goblet cells, while the bulbar conjunctival surface contained a stratified columnar epithelium with three to five layers of epithelial cells with numerous goblet cells, which were strongly PAS and Alcian blue pH 2.5 positive. In red kangaroos, dogs and wild ruminants, the bulbar conjunctiva consisted of a non-keratinised stratified squamous epithelium with goblet cells (Al-Ramadan, 2015;Al-Ramadan & Ali, 2012;Cazacu, 2010;Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Krasucki, et al. 2015, Klećkowska-Nawrot, Nowaczyk, Goździewska-Harłajczuk, Szara, et al. 2015). ...
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This study described the anatomy, histology and the histochemical analysis of the eye tunics, the upper and lower eyelid, the third eyelid, the lacrimal gland and the superficial gland of the third eyelid in adult Sulawesi bear cuscus. The eyeball and the eyelids with the orbital glands were harvested immediately post-mortem. The eyeball in the Sulawesi bear cuscus had a sphere-like shape. The pupil was round, and the lens was a circular biconvex body. There was neither tapetum lucidum nor Harderian gland. Similarly, there were no eyelashes in the lower eyelid. The lymphoid follicles and the high endothelial venules (HEV) were found in the lymphoid region only in the third eyelid and in the connective tissue of the superficial gland of the third eyelid. The third eyelid in the bear cuscus resembled the letter “T.” The lacrimal gland and superficial gland of the third eyelid were multilobar tubuloacinar glands. The histological analysis and histochemical studies showed that the lacrimal gland in the Sulawesi bear cuscus produced a mucoserous secretion with predominantly serous cells. In contrast, the superficial gland of the third eyelid produced a serous secretion with a single acinus mucous in character.
... Studies on the morphology of the eyelids have been carried out in numerous domestic and wild animals, including ruminants, carnivores, horses, pigs, the Indian mongoose, pinnipeds, primates and chickens (Dyce et al. 1996;Ankel-Simons 2000;Nickel et al. 2004;Yasui et al. 2006;Al-Ramadan & Ali 2012;Kelleher Davis et al. 2013;Kamali et al. 2015). The majority of those studies were performed on guinea pigs (Latkovic 1979a,b;Latkovic & Nilsson 1979a, 1979bGasser et al. 2011), rats (Setzer et al. 1987;Huang et al. 1988) and mice (Findlater et al. 1993;Smith et al. 2002). ...
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The upper, lower and third eyelids are accessory organs of the eye. The aim of this study was to describe the development of the upper, lower and third eyelids in ostriches in the embryonic and postnatal period and to characterise the conjunctiva-associated lymphoid tissue (CALT) in the eyelids. The study was performed on 59 African black ostriches from the 28th day of incubation up to 3 years of age. Hematoxylin and eosin, Azan trichrome, van Gieson trichrome and Mallory’s trichrome stainings were used to demonstrate the structure of the eyelids. The connective tissue structure transformed from loose connective tissue into dense connective tissue during the development of the eyelids. In the third eyelid, the network of collagen fibres was rebuilt and the density of the collagen fibres decreased with age. As the animals grew, there were clearly visible changes in the structure of the upper and lower eyelids, especially in the stratified squamous epithelium of the skin surface, the conjunctival epithelium and the tarsal plate. The lymphatic follicles were observed only in the lower eyelid of adult ostriches. A diffuse CALT system with scattered lymphatic cells was observed within the connective tissue of the third eyelid, mostly under the conjunctival epithelium in the group of adult birds.
... From available literature, the morphology of dorsal lacrimal glands of humans (Draper et al., 1999;Obata, 2006); cattle , Camel (Mohammadpour, 2008;Al-Ramadan and Abdelhadi, 2012), dogs (martin et al., 1988), pigs (Klećkowska-Nawrot and Dziegiel, 2008Henker et al., 2013) , rabbits (Michele et al., 1994;Rehorek, 2011), sheep (Garguilo et al., 2000ElHafez et al., 2014), and rats (Draper et al., 1998) has been described. There is, however, dearth of information about the histomorphology dorsal lacrimal gland of the African palm squirrel in available literature. ...
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The conjunctiva is important adnexa of the eye that maintains the stability of the tear film. The objective of current study is to describe the histological features of palpebral conjunctiva of the dromedary, emphasizing the distribution of Muc1 using indirect tissue immunofluorescence technique. Conjunctival samples of ten adult, apparently healthy dromedary camels of both sexes were collected, fixed, embedded in paraffin and stained with H&E for general histological structure, Masson´s trichrome for fibrous tissue, Periodic acid–Schiff (PAS) for goblet cells and immunofluorescence for the distribution of Muc1. The palpebral conjunctiva of the dromedary camel is lined with stratified squamous to stratified columnar epithelium. Large numbers of goblet cells were identified associated with conjunctival epithelial cells. The lamina propria consisted of loose superficial cell layer and a deeper tarsal plate. Within the lamina propria, there were lymphoid follicles, numerous tarsal glands and palpebral seromucoid glands. The palpebral conjunctiva and associated palpebral glands were stained positive for PAS and Muc1. In conclusions, the eye of the dromedary camel is protected with a palpebral conjunctival tissue that is richly populated with PAS positive cells and numerous Muc1-producing cells.
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