Download a gross anatomical study of the lacrimal apparatus of the camel

A GROSS ANATOMICAL STUDY OF THE LACRIMAL APPARATUS OF THE CAMEL
(Camelus dromedarius)
BY
1
2
Z. H. M. A. Ibrahim , A. B. Abdalla and D. I. Osman 2
1- Department of Anatomy, College of Veterinary Medicine and Animal Production, Sudan University for Science and
Technology. 2- Department of Anatomy, Faculty of Veterinary Medicine, University of Khartoum.
ABSTRACT
A gross anatomical study was made on the lacrimal apparatus in seventeen
adult camels (4-10 years age), and three foetuses. The lacrimal gland is situated
between the caudodorsal aspect of the eyeball and the supraorbital and frontal process
of the frontal and zygomatic bones, respectively. The gland consists of two lobes,
cranial and caudal. The excretory ducts were 3-4 in number, and opened into the
superior conjunctiva. There were no puncta lacrimalia, either in the lower, or the
superior eyelid. The two lacrimal ducts started blindly and opened into the lacrimal
sac, the enlarged beginning of the nasolacrimal duct. The nasolacrimal duct begins as
a small osseous duct in the bony lacrimal canal and continues rostrally medial to the
maxilla. It opens into the medial wall of the nasal vestibule at the junction of the skin
with the mucous membrane. In its course the nasolacrimal duct has many fenestrae in
its wall. The arterial supply to the lacrimal gland comes from the lacrimal artery, a
branch of rete mirabili of the external ophthalmic artery, and it is drained by the
lacrimal vein which joins the ophthalmic vein.
:‫ﻤﻠﺨﺹ‬
10-4 ‫ )ﻓـﻲ ﻋﻤـﺭ‬،‫ﺃﺠﺭﻴﺕ ﻫﺫﻩ ﺍﻝﺩﺭﺍﺴﺔ ﺍﻝﺘﺸﺭﻴﺤﻴﺔ ﻋﻠﻰ ﺍﻝﺠﻬﺎﺯ ﺍﻝﺩﻤﻌﻲ ﻓﻲ ﺴﺒﻌﺔ ﻋﺸﺭ ﻤﻥ ﺍﻹﺒل‬
‫ ﺘﺘﻭﻀﻊ ﺍﻝﻐﺩﺓ ﺍﻝﺩﻤﻌﻴﺔ ﺒﻴﻥ ﺍﻝﻨﺎﺤﻴﺔ ﺍﻝﺫﻴﻠﻴﺔ ﺍﻝﻅﻬﺭﻴﺔ ﻝﻠﻤﻘﻠﺔ ﻭﺍﻝﺸﺎﺨﺼﺔ ﻓﻭﻕ ﺍﻝﺤﺠﺎﺝ‬.‫ ﻭﻜﺫﻝﻙ ﻓﻲ ﺜﻼﺜﺔ ﺃﺠﻨﺔ‬،(‫ﺴﻨﺔ‬
‫ ﻗﻨﻭﺍﺕ ﺍﻹﻓﺭﺍﻍ ﻋـﺩﺩﻫﺎ ﻤـﻥ‬.‫ ﺍﻝﻔﺹ ﺍﻝﻘﺤﻔﻲ )ﺍﻝﺭﺌﻴﺴﻲ( ﻭﺍﻝﻔﺹ ﺍﻝﺫﻴﻠﻲ‬:‫ ﺘﺘﻜﻭﻥ ﺍﻝﻐﺩﺓ ﻤﻥ ﻓﺼﻴﻥ‬.‫ﻝﻠﻌﻅﻡ ﺍﻝﺠﺒﻬﻲ‬
‫ ﺘﺒـﺩﺍ ﺍﻝﻘﻨﺎﺘـﺎﻥ‬.‫ ﻻ ﺘﻭﺠﺩ ﻨﻘﻁﺔ ﺩﻤﻌﻴﺔ ﺒﺎﻝﺠﻔﻥ ﺍﻝﻌﻠﻭﻱ ﺃﻭ ﺍﻝﺴﻔﻠﻲ‬.‫ ﻭﺘﻔﺘﺢ ﻓﻲ ﻗﺒﻭﺍﻝﻤﻠﺘﺤﻤﺔ ﻓﻲ ﺍﻝﺠﻔﻥ ﺍﻝﻌﻠﻭﻱ‬4-3
‫ ﺘﺒﺘـﺩﺉ‬.‫ ﻭﻫﻭ ﺍﻝﺠﺯﺀ ﺍﻝﻤﺘﻀﺨﻡ ﻤﻥ ﺍﻝﻘﻨﺎﺓ ﺍﻷﻨﻔﻴﺔ ﺍﻝﺩﻤﻌﻴﺔ‬,‫ﺍﻝﺩﻤﻌﻴﺘﺎﻥ ﻜﻘﻨﺎﺘﻴﻥ ﻋﻭﺭﺍﺘﻴﻥ ﺘﻔﺘﺤﺎﻥ ﻓﻲ ﺍﻝﻜﻴﺱ ﺍﻝﺩﻤﻌﻲ‬
‫ﺍﻝﻘﻨﺎﺓ ﺍﻷﻨﻔﻴﺔ ﺍﻝﺩﻤﻌﻴﺔ ﻜﻘﻨﺎﺓ ﺼﻐﻴﺭﺓ ﺩﺍﺨل ﺍﻝﻘﻨﺎﺓ ﺍﻷﻨﻔﻴﺔ ﺍﻝﺩﻤﻌﻴﺔ ﺍﻝﻌﻅﻤﻴﺔ ﻭﺘﻤﺭ ﺍﻨﺴﻴﺎ ﻝﻠﻔﻙ ﺍﻝﻌﻠﻭﻱ ﻝﺘﻔﺘﺢ ﻓﻲ ﺍﻝﺠﺩﺍﺭ‬
‫ ﺍﻹﻤـﺩﺍﺩ ﺍﻝـﺩﻤﻭﻱ‬.‫ ﺠﺩﺍﺭ ﺍﻝﻘﻨﺎﺓ ﺒﻪ ﻓﺘﺤﺎﺕ ﻓﻲ ﻤﺴﺎﺭﻩ‬.‫ﺍﻹﻨﺴﻲ ﻝﺩﻫﻠﻴﺯ ﺍﻷﻨﻑ ﻋﻨﺩ ﺍﻝﺘﻘﺎﺀ ﺍﻝﻐﺸﺎﺀ ﺍﻝﻤﺨﺎﻁﻲ ﺒﺎﻝﺠﻠﺩ‬
‫ ﺘﺼﺭﻑ ﺍﻝﻐـﺩﺓ‬.‫ﻝﻠﻐﺩﺓ ﺍﻝﺩﻤﻌﻴﺔ ﻴﺄﺘﻲ ﻤﻥ ﺍﻝﺸﺭﻴﺎﻥ ﺍﻝﺩﻤﻌﻲ ﻭﻫﻭ ﻓﺭﻉ ﻤﻥ ﺍﻝﺸﺒﻜﺔ ﺍﻝﻌﺠﻴﺒﺔ ﻝﻠﺸﺭﻴﺎﻥ ﺍﻝﻌﻴﻨﻲ ﺍﻝﺨﺎﺭﺠﻲ‬
.‫ﺒﺎﻝﻭﺭﻴﺩ ﺍﻝﺩﻤﻌﻲ ﺍﻝﺫﻱ ﻴﺘﺼل ﺒﺎﻝﻭﺭﻴﺩ ﺍﻝﻌﻴﻨﻲ‬
INTRODUCTION
In its harsh environment, the dromedary camel is subjected to lack of feed and
water, and other problems of hot and dry climate. Adaptation of the camel to this
inhospitable environment has come through certain behavioral, physiological and
anatomical characteristics. Since it is well known that the lacrimal gland secretes a
watery secretion, the morphological study of the lacrimal gland may contribute a
great deal to a better understanding of the problem of water loss and conservation in
the dromedary.
The anatomy of the dromedary lacrimal apparatus has not previously been
clearly established, and the few references available in the literature are of rather
general kind. Thus Leese (1927) stated that the lacrimal puncta were exceedingly
small, and Awkati and Al-Bagdadi (1971) concluded that the lacrimal gland in the
camel is comparatively less developed than that of the horse or ox. Abdalla, Fahmy
and Arnautovic (1970) and Saber and Makady (1987) deny the existence of puncta
lacrimalia in the camel.
MATERIALS AND METHODS
A total of twelve heads of adult camels and three heads of foetuses near term
were used for the study of the topographical anatomy of the lacrimal apparatus. For
the study of the blood supply of the lacrimal gland five heads of adult camels were
used. The heads of adult camels were separated. Some of the heads were put in a
freezer chest, and others were perfused. The perfusion was made first with normal
saline injected into the right and left common carotid arteries, followed by 10%
formalin. The heads were immersed in the same solution and left for later dissection.
To determine the weight of the gland, fresh specimens were used. The whole gland
was carefully dissected out and weighed on a sensitive balance. Measurements of the
dimensions of the gland were also made. Measurements of the gland were carried out
both on fresh and fixed specimens. To expose the lacrimal ducts, lacrimal sac, and
nasolacrimal duct injection of coloured resin (vinylite) was made into the nasal
opening of the nasolacrimal duct.
The study of the blood vessels of the lacrimal gland, resin was again used. To
trace arteries of the gland 10% green or yellow vinylite was injected into the right and
left common carotid arteries. The veins were demonstrated by careful dissection.
After the completion of the injections, the heads were preserved in 10% formalin or
deep freezed. Dissection of the vessels was started after the resin had set.
RESULTS
Position and Relationships of the Lacrimal Gland: The lacrimal gland was situated within a
special division of the periorbita between the caudodorsolateral part of the eyeball and
the supraorbital process of the frontal bone and the frontal process of the zygomatic
bone (Figs.1, 2).
(Fig.1): A tracing showing the Right Lacrimal Apparatus in the Skull of the Camel. Notice the Gland (1)
with its caudal Prolongation (2) and the Excretory Ducts (3), the Lacrimal Ducts (4), Lacrimal Sac (5),
Nasolacrimal Duct (6) and Level of its Opening (7).
The major part of the gland was covered by the supraorbital and frontal
processes dorsally, whereas a small caudal part (about 1cm wide) was covered only
by adipose tissue, fascia and skin.
The ventral surface lay on the caudodorsolateral surface of the eyeball from
which it was separated by the periorbita. The rostromedial margin of the gland was
situated sagitally to the supraorbital process. The rostrolateral margin was situated
along the rostral border of the frontal process, whereas the basal margin was situated
about 10mm from the caudal margin of the supraorbital process (Fig.1). The rostral
angle was situated about 5mm from the middle of the rostral margin of the
supraorbital process, the lateral angle at the margin of the frontal process, and the
caudal angle at the root of the supraorbital process.
A separate accessory gland was found in two of the specimens investigated.
The accessory gland was situated 10mm cranial to the rostrolat-eral margin of the
lacrimal gland.
(Fig. 2): A Diagram Showing the Different Constituents of the Lacrimal Apparatus: 1. Lower Eyelid. 2.
Upper Eyelid. 3. Lateral Canthus. 4. Lacrimal Gland. 5. Excretory Duct. 6. Upper Lacrimal Duct. 7. Lower
Lacrimal Duct. 8. Lacrimal Sac. 9. Nasolacrimal Duct.
The lacrimal gland was light brown in colour. It
was difficult to distinguish it from the surrounding muscles of the eyeball. The shape of
the gland was an irregular triangle, but occasionally the gland was crescent-shaped.
The gland consisted of two lobes connected by a connective tissue sheath (Fig.3). The
main (cranial) and small (caudal) lobes were irregularly triangular in shape.
Although the gland consisted of two lobes, it appeared as one unit which had
two surfaces, three margins, and three angles (Figs.1, 3). The dorsal surface was
convex in conformity with concavity of the bony orbit. The ventral surface was
concave, being adapted to the convex eyeball. The rostromedial and rostrolateral
margins were irregular, whereas the caudal margin followed the caudal margin of the
frontal process.
In a few specimens there was a prolongation of the gland about 10mm from
the medial half of the base of the triangle.
Weight and Dimensions: The weight of the lacrimal gland ranged between 1.95 and
2.49gm.
As a single unit the gland measured 55mm in length, and 20mm in width. The
length of the cranial lobe was 35mm, and the width 20mm. The caudal lobe was
20mm in length and width. The thickness of the gland varied between 5mm in the
middle of the cranial lobe and 2mm in the most lateral aspect of the caudal lobe and
the most medial part of the cranial lobe.
Colour and Shape of the Lacrimal Gland:
(Fig.3): The isolated left lacrimal gland. The lobulation of the gland is clear. Notice the cranial lobe (1), the
caudal lobe (2) and the connective tissue in between. (3).
The Excretory Ducts: The gland possessed 3 - 4 excretory ducts. The cranial lobe had 12 ducts, whereas the caudal lobe had a single duct. In those specimens with an
accessory gland, there was one duct from the accessory one. The excretory ducts
emerged from the ventral surface of the corresponding part of the gland, ran parallel
to each other, penetrated the periorbita, and opened anterior to the fornix of the
conjunctiva of the upper eyelid (Fig.1). The ducts were small and difficult to find but
were detected by the black colour imparted to them by melanin. Each duct was about
12mm in length.
The Lacrimal Ducts: The lacrimal puncta were absent in all the specimens studied. The
lacrimal ducts thus began blindly at the medial part of the border of the upper and
lower eyelids (Figs.1, 2). Each lacrimal duct was about 10mm long; it opened into the
lacrimal sac after penetrating the periorbital tissue. In three of the specimens
investigated the two lacrimal ducts joined to form a common duct which opened into
the sac.
The Lacrimal Sac: The lacrimal sac was located in the lacrimal fossa of the lacrimal
bone (Figs.2, 4). The sac was funnel-shaped. Its palpebral part was concave as it was
pressed against the convex eyeball. The outer surface was convex in adaptation to the
concavity of the lacrimal fossa. The sac measured 15mm transversely and 5mm
sagitally. The sac was blind dorsolaterally, and received medially and laterally the
corresponding lacrimal ducts. Rostroventr-ally it was continuous with the
nasolacrimal duct.
Fig. (4): Avinylite Cast of the Lacrimal Sac and Nasolacrimal Duct Showing the Lacrimal Sac (1) and the
Nasolacrimal Duct (2).
The duct originated from the lacrimal sac, and was about
200mm long. Its initial part, about 10 – 15mm, was situated in the osseous lacrimal
The Nasolacrimal Duct:
canal (Figs.1, 2, 4). It parted from the osseous canal at the caudal portion of the
ventral nasal meatus, ventral to the maxilloturbinate crest. It then passed forwards
under the mucous membrane of the ventral nasal meatus medial to the maxilla and the
nasal process of the premaxilla. At the level of the nasal process of the premaxilla the
duct underwent a slight dilatation. It opened into the medial wall of the nasal vestibule
at the junction between the mucous membrane and skin. The nasal opening of the
nasolacrimal duct was difficult to detect. The oval opening lay about 10mm medial to
the wider opening of the blind sac. The duct had many fenestrae in its wall along its
course distal to the osseous canal.
The Blood Vessels: The lacrimal gland received its arterial supply from the lacrimal
artery which was a branch of the rete mirabili of the external ophthalmic artery. The
artery ran lateral to the lacrimal nerve, pierced the periorbita to reach the gland at its
caudolateral part. It supplied both cranial and caudal lobes. It also supplied the
conjunctiva of the upper eyelid.
The venous drainage was by the lacrimal vein which joined the ophthalmic
vein. The latter- mentioned drained into the maxillary vein and finally into the
external jugular vein.
DISCUSSION
It appears from the present study that the position of the lacrimal gland of the
camel is similar to that reported in the same species by Addalla et al., (1970), Awkati
and Al-Bagdadi (1971). The present study also supports the findings of Abdalla et al.,
(1970) that the major portion of the gland is applied to a shallow depression of the
supraorbital process whereas a small caudal process is covered only by adipose tissue.
In other domestic mammals the position of the lacrimal gland is similar to that
in the camel. For example, in the pig (Sisson and Grossman, 1975), horse (Bradley,
1946; Sisson and Grossman, 1975), ox (Sisson and Grossman, 1975), and small
ruminants (Sinha and Calhoun, 1966) the lacrimal gland is situated on the dorsolateral
aspect of the eyeball, covered by the zygomatic process of the frontal bone. In both
the horse (Sisson and Grossman, 1975), and the ox (Diesem, 1968; Sisson and
Grossman, 1975) the gland is partially covered with fat.In man the lacrimal gland is
also located between the superiolateral angle of the bony orbit and the eyeball
(Starling and Evans, 1968; Agur and Lee, 1991).
The colour of the lacrimal gland of the camel is light brown in the fresh state.
This agrees with the findings of Al-Ani (1997) in the same species. However, the
colour varies between red in the dog (Bradley, 1948; Miller, 1962) and pink in the
small ruminants (Sinha and Calhoun, 1966). It is probable that the variation in the
colour depends on the degree of bleeding, especially so in those animals in which the
gland is examined after the slaughtering of the animal.
The shape of the gland is evidently determined by its position. Thus in the
camel the gland is convex dorsally in conformity with the convexity of the bony orbit.
It is irregular in shape. These findings agree with those of Abdalla et al., (1970). In
other domestic mammals the gland varies in shape between species. It is triangular in
pig, and bipartite in ox, sheep and goat (Sisson and Grossman, 1975). In man the
lacrimal gland is bipartite, the two parts being connected with each other by the
aponeurosis of the levator palpebrae superioris (Warwick and Williams, 1973;
Romanes, 1986). According to the latter-mentioned authors, there are numerous
accessory lacrimal glands opening into the conjunctival fornices, especially the
superior one. It seems that the shape of the gland depends not only on the
relationships of the gland but also on the degree of development of the gland itself.
The weight of the lacrimal gland of the camel is about 1.97g. It is interesting
to note that for so big an animal the gland is so small in size. This has already been
commented on by Awkati and Al-Bagdadi (1971) who state that the lacrimal gland of
the camel is less well-developed than that of either the ox or horse. Thus the statement
by Sisson and Grossman (1975) that the size of the lacrimal gland is related to animal
size may not be universally true. The lacrimal gland of the camel measures about 55
mm in length and about 20 mm in width. Abdalla et al., (1970), however, report
dimensions of 40 mm for length and 20 mm for width. Moreover, Awkati and AlBagdadi (1971) stated that the lacrimal gland of the camel is 45 mm in length and 24
mm in width. The discrepancy in these reported measurements may be explained by
differences in the age of the animal studied.
The present study reveals that the number of excretory ducts of the lacrimal
gland is 2 – 4. This confirms the findings of Abdalla et al., (1970). However, Awkati
and Al-Bagdadi (1971), Zaid, Ghadiri and Shareeha (1991), and Al-Ani (1997) all
claimed that the number of excretory ducts of the lacrimal gland of the camel is two.
Moreover, both Awkati and Al-Bagdadi (1971) and Al-Ani (1997) stated that the two
ducts, one thick and the other thin, unite, forming a single duct that open into the
superior fornix. In other domestic mammals there is also some variation in the number
of excretory ducts. Fore example in the dog (Sisson and Grossman, 1975), ox (Sisson
and Grossman, 1975) and small ruminants (Sinha and Calhoun, 1966) the number of
excretory ducts is 12–16, 6–8, and 2–5 respectively. This variation in the number of
excretory ducts, between and within the same species may be explained by normal
variation, and also by the fact that these ducts are small and can not readily be seen. It
is possible to detect them, however, by careful dissection and by observing the often
heavy pigmentation of their lining epithelium.
In most of he domestic mammals each of the two lacrimal ducts starts by a small
one upper and one lower opening, the punctum lacrimale, situated close to the medial
angle of the respective eyelid. The present study confirms the findings of Abdalla et
al., (1970) and Saber and Makady (1987) that the puncta of the camel are absent, and
that the lacrimal ducts start blindly. Leese (1927) states that the puncta are
exceedingly small and can not be probed. In the llama, a member of Camelidae, the
puncta are patent (Sapienza, Isaza, Jonson and Miller, 1992). The absence of the
puncta, or at least one of them is not a feature unknown among the domestic
mammals. In the pig (Sisson and Grossman, 1975) and in the dog (Dyce, Sack, and
Wensing, 1987) one punctum, the lower one in case of the pig, may be absent, so that
the lacrimal punctum is not functional. The absence of one, or the other, of the
lacrimal puncta in some mammals does not entierly deprive the nasal mucosa of the
moistening effect of the lacrimal fluid, but in the camel that moistening effect is
excluded by the absence of the puncta. The absence of the puncta causes excess
lacrimal fluid to escape by flowing over the lower eyelid. This probably explains the
popular myth that the camel is so emotional that it sometimes (sheds tears).
The lacrimal sac which is the enlarged beginning of the nasolacrimal duct, is
funnel-shaped and is situated in a fossa of the lacrimal bone. This confirms the
findings of Abdalla et. al., (1970). The sac is absent in the pig (Sisson and Grossman,
1975). Marcenac and Olivier (1953) deny the existence of a lacrimal sac in the dog. In
man there is always a lacrimal sac which lies in the fossa formed by the lacrimal and
maxillary bones (Warwick and Williams, 1973; Romanes, 1986) or in the lacrimal
groove behind the medial palpebral ligament (Snell, 2000).
In all mammals in which the puncta lacrimalia are present the nasolacrimal
duct carries the surplus lacrimal fluid to the nasal cavity. In mammals also the caudal
portion of the duct is in a bony canal. The rostral portion is covered only by the nasal
mucosa.
In the present study the nasolacrimal duct, about 200 mm long, is situated in
the osseous lacrimal canal; it leaves the canal at the caudal part of the ventral nasal
meatus, ventrolateral to the maxilloturbinate crest. The ducts open into the medial
wall of the nasal vestibule at the junction of the mucous membrane and the cutaneous
epithelium. The opening is difficult to detect. The remarkable feature of the
nasolacrimal duct is the existence of many breaks in its wall distal to the bony canal.
It has been mentioned above that the nasolacrimal duct of the camel is not functional
and, therefore, no lacrimal fluid is carried to the nasal cavity. The presence of defects
in the wall of the nasolacrimal duct is a common feature in the pig, mule and ox
(Sisson and Grossman, 1975). In the pig (Sisson and Grossman, 1975) the middle
portion of the duct is incomplete for a distance of about 30 – 70 mm and the only
functional part is the portion of the duct that travels in the bony canal. This
assumption may, however, be incorrect. The presence of breaks in the nasolacrimal
duct may be a device to allow the lacrimal fluid to escape, and to moisten the caudal
portion of the nasal cavity where these breaks occur. The existence of these breaks is
not necesserily a proof that no lacrimal fluid passes into the rostral portion of the duct.
In the camel, too, breaks occur in the wall of the nasolacrimal duct. Although in the
camel lacrimal fluid does not flow through the nasolacrimal duct, the presence of the
fenestrae in the wall may merely suggest a developmental preservation of a feature
not uncommon in mammals.
The present study shows that the arterial supply to the lacrimal gland comes
from the lacrimal artery, a branch of the rete mirabili of external ophthalmic artery.
This confirms the findings of Kanan (1972), and Smut and Bezuidenhout (1987) in
the camel. The lacrimal artery runs lateral to the lacrimal nerve, pierces the periorbita
and supplies the whole of the gland and also the conjunctiva of the upper eyelid. This
pattern of origin and distribution of the lacrimal artery of the camel conforms in
general to the pattern in other domestic mammals. However, in the ox, sheep and goat
(Sinha and Calhoun, 1966; Sisson and Grossman, 1975) another lacrimal artery may
arise from the superficial temporal artery. On the other hand the lacrimal artery in
man is a branch of the internal carotid artery (Dyce et. al., 1987).
In this study and in that by Smut and Bezuidenhout (1987) the venous
drainage of the lacrimal apparatus is by the lacrimal vein, a tributary of the
ophthalmic vein, which drains into the maxillary vein. It seems that in some mammals
the venous pattern is somewhat variable. In the horse, for example, the lacrimal vein
is a tributary of the supraorbital vein (Diesem, 1968); the blood then goes to the
ophthalmic vein.
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