Global Veterinaria 9 (6): 691-695, 2012 ISSN 1992-6197 © IDOSI Publications, 2012 DOI: 10.5829/idosi.gv.2012.9.6.66187

Topographical and Morphological Anatomy of the Guttural Pouches of the Domestic Donkey (Equus asinus)

1Seyed Morteza Ghazi, 2Behzad Mobini and 2Mohammad Reza Afsharzadeh

1School of Veterinary Medicine, Islamic Azad University, Shahrekord Branch, Shahrekord - Iran 2Department of Basic Sciences, College of Veterinary Medicine, Islamic Azad University, Shahrekord Branch, Shahrekord - Iran

Abstract: Guttural pouches are paired filled with air, located ventral to the atlas. The donkeys possessed large, symmetrical guttural pouches incompletely divided into medial and lateral compartments by the stylohyoid bone. The left and right guttural pouches have almost the same capacity. In this study, topographic and morphologic anatomy of the left and right guttural pouches was carried out in the heads of male and female healthy donkeys. Results of the transverse and median sections of the heads revealed that the guttural pouches of donkey were much smaller than those of the horse. All the anatomical structures related to the guttural pouches of donkey resemble those in the horse with differences in the pharyngeal recess which was deeper and larger in donkey. The lateral walls of each guttural pouch contain the five (VII, IX, X, XI and XII), the cranial cervical ganglion, the cranial sympathetic trunk, the cranial laryngeal and pharyngeal nerves and the linguofacial trunk, maxillary vein, the internal carotid and branches of the external carotid arteries. The volumes of the guttural pouches in the males were larger than females. The length, width and depths of the lateral compartment in right side were more than left guttural pouch, while these values for medial compartments were reversed. The retropharyngeal lymph node which located under the floor of guttural pouch was found in both sexes.

Key words: Anatomy % Donkey (Equus asinus) % Guttural Pouch % Morphologic % Topographic

INTRODUCTION Because of their localization and relationship with several cranial nerves and blood vessels, the pouches The guttural pouches are large paired auditory tube are of veterinary importance in perissodactyls [3, 6, 7]. diverticuli present in the horse as well as in other The diseases of the guttural pouch such as emphysema, mammals [1, 2], such as horse, donkey, tapir [3, 4]. mycosis, tympany, neoplasia, cysts and muscle ruptures The pouches are symmetrically extended from the can result in erosion of the carotid artery and precipitate to the atlanto-occipital joint in both sides fatal hemorrhages [11, 12], or make the pouch susceptible [5-8]. The right and left guttural pouches met each to serious clinical conditions [5]. other at the median part to form a thin membranous Although, some advanced studies give adequate septum. Moreover, each pouch incompletely divided detail on the topographic and morphologic anatomy of into medial and lateral compartments by the stylohyoid the guttural pouch of the horse [4, 7, 9, 13, 14], to our bone [5]. knowledge there are limited reports in the literature The physiological function, if any, of guttural pertaining to the topographic and morphologic anatomy pouches is unknown, but recently it has been proposed of the guttural pouch of the donkey [15]. Therefore, that they might have an important function of brain this study was undertaken to investigate more precisely cooling [3, 5, 9] and also intimately involved in the the anatomical features of the guttural pouches of the physiology of swallowing [4, 10]. donkey bilaterally.

Corresponding Author: Behzad Mobini, Department of Basic Sciences, College of Veterinary Medicine, Islamic Azad University, Shahrekord Branch, Shahrekord - Iran. Tel: +98-311-7754770, Fax: +98-381-3361060. 691 Global Veterinaria, 9 (6): 691-695, 2012

MATERIALS AND METHODS Oto and Haziroglu [19] and Manglai et al. [7] described that the dorsal side of the pouches consisted Four healthy adult donkeys for teaching purpose in of hard tissue (sphenoid bone and occipital bone) and the Department of Anatomy, College of Veterinary except for the region connected to the stylohyoid bone, Medicine, Shahrekord Islamic Azad University, the other walls were in contact with soft tissue such as Shahrekord, Iran, were used in this study (2 each sex). pharynx, esophagus and many muscles. Similar findings Euthanization were made by using 20ml of Acepromazine were observed in this study. (2%; Alfason, Woerden, Holland) as a sedative and 250ml The results of topographic anatomy showed that of Magnesium sulfate (29.1%, Sahand, Tabriz, Iran). the pharyngeal recess in the donkey was deep and large. The guidelines of the ethical committee of Shahrekord This finding agrees with those reported by Alsafy et al. Azad University were strictly followed during the [15] and Lindsay and Clayton [22]. It has been shown to procedure. All the heads were cut off transversely at the have a close physical relation with the medial laminae and level of the sixth cervical vertebra. Transverse section of septum of the auditory tube diverticula. It is equally the donkey’s head passed at the level of the medial likely, therefore, that the excursions of the recess reflect canthus of the eyes, whereas median section passed pressure changes within the auditory diverticula and that longitudinally on the head. The volume, the maximum the asymmetric movements of its wall are due to differing length, width and depth of the right and left pouches pressures in the two diverticula [22]. were measured in both sexes. The specimens were The , the linguofacial trunk, submerged in 10% formalin and dissection was performed the cranial cervical ganglion, the cranial sympathetic carefully on the anatomical structures related to the trunk, the cranial laryngeal and pharyngeal nerves, as guttural pouches. Definitions of the anatomical structures well as the , glossopharyngeal N., vagus N., were based on the atlases regarding accessory N., hypoglossal N., branches of the external [16, 17, 18]. All steps were photographed by digital camera carotid and maxillary vein were present in the lateral walls (Sony, Cyber-shot, DSC-H10). of the guttural pouches (Figs. 2-4). These results are in agreement with those recorded previously [5, 7, 15, 19, 23]. RESULTS AND DISCUSSION The total mean volume of the guttural pouches in the male donkeys was more (195 ml) than that in the The current study demonstrated that donkeys females (185 ml). This may be due to the bray mechanism. possessed relative large symmetric guttural pouches It is believed that a remarkable large size of pharyngeal which extended from the pharynx to the atlanto-occipital recess plays a role in braying [22]. joint in both sides [5-8, 15, 19]. The capacity of the right and left guttural pouch in Manglai et al. [7] described the opening of auditory male donkeys were respectively 164 ml and 227 ml, tube as a funnel form canal. On the contrary, Oto and whereas in the females were 190 and 180 ml, respectively. Haziroglu [19] emphasized that the entrance of the The different values for the capacity of the right and left pharyngeal part of the pouches was like a triangle shape guttural pouches may be due to the deviation of the head orifice. In this study, it clearly observed parallel data to to the right or left during euthanization. Since declination Oto and Haziroglu [19]. of the head to the right or left reduces the volume of the Each pouch incompletely divided into medial and right or left guttural pouches, accordingly. lateral compartments by the stylohyoid bone. They lie Although, Lepage [21] has stated that the capacity between the base of the skull (basilar part of the occipital of guttural pouches in horses were generally ranged from and sphenoid bones) and atlas dorsally, the pharynx, 300 to 600 ml, but Manglai et al. [7] reported that the retropharyngeal lymph node and commencement of the capacity of guttural pouches in adult horses were 472 cm3. esophagus ventrally, the parotid and mandibular salivary In comparison of the capacity of guttural pouches in glands, caudal belly of the digastric and pterygoideus horses with donkey, It was determined that the donkeys medialis muscles, laterally. In the medial plane, the left possessed smaller guttural pouches than horses. and right sacs were separated from each other by the The average length, width and depths of the lateral rectus capitis ventralis and longus capitis muscles (Fig. 1). compartments of the right guttural pouches (24.65 cm, These results are in agreement with those recorded 5.10 cm 2.85 cm, respectively) were more than those in previously [3, 5, 15, 16, 19-21]. left side (23.45 cm, 5.05 cm and 2.35 cm, respectively),

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Fig. 1: The topography of the guttural pouch (G.P) and close structures in the donkey. Medial view, right lateral compartment (R.L.C), right medial compartment (R.M.C), left medial compartment (L.M.C) left lateral compartment (L.L.C), pharynx (P), larynx (L), basisphenoid bone (B.S), basilar part of occipital bone (B.O), rectus capitis ventralis muscle (R.C.V), atlas (A), pterygoideus medialis muscle (P.M), pharyngeal orifice of auditory tube (P.O.A.T), spinal cord (S.C), nasopharynx (N.P), pharyngeal recess (P.R), stylohyoid bone (S), sphenoidal sinus (S.S), (S.P), frontal sinus (F.S)

Fig. 2: Median section of the head of a donkey. basisphenoid bone (B.S), internal carotid a. (I.C.A), retropharyngeal lymph node (R.P.L.N), linguofacial trunk (L.T), (H.G.N), guttural pouch (G.P)

Fig. 3: Median section of the head of the donkey passes at the level of the middle of the nuchal crest, atlas and axis bones. Stylopharyngeus caudalis muscle (S.C.M), occipitohyoideus muscle (O.H.M), hypoglossal nerve (H.G.N), maxillary vein (M.V), pharyngeal nerve (P.N), pharynx (P)

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Fig. 4: The guttural pouch and its related structures in the donkey. Medial view, hypoglossal nerve (H.G.N), glossopharyngeal nerve (G.P.N), (A.N), (V.N), maxillary vein (M.V) while these values in the medial compartments of the left 4. Sasaki, M., Y. Hayashi, H. Koie, Y. Yamaya, guttural pouches (30.40 cm, 5.55 cm and 2.05 cm, J. Kimura, D. Manglai, S. Kawashima, H. Endo and respectively) were more than those in right side (29.20 cm, M. Yamamoto, 1999. CT examination of the guttural 5.25 cm and 2.10 cm, respectively). pouch (auditory tube diverticulum) in Przewalski’s Oto and Haziroglu [19] and Carmalt [5] reported that horse (equus przewalskii). Journal of Veterinary the medial compartment was larger than the lateral part. Medical Science, 61: 1019-1022. On the contrary, Manglai et al. [7] emphasized that the 5. Carmalt, J., 2002. Guttural pouch diseases in the lateral compartment was wider and medial part was horse. Large Animal Veterinary Rounds, Vol 2, narrow. We clearly observed that the medial compartment Issue 2, EriÕim: [http:// www.drounds.ca/ crus/ was a little bigger than that of the lateral part. laveng_0202.pdf], EriÕim tarihi: 15.09.2009. 6. Liebich, H.G. and H.E. König, 2004. Vestibulocochlear CONCLUSIONS Organ. In: Veterinary Anatomy of the Domestic Mammals, 4th ed., König, H.E. and Liebich, H.G. eds., The results of topographic and morphologic Schattauer, Stuttgart, pp: 577-579. anatomy demonstrated that the guttural pouches of 7. Manglai, D., R. Wada, H. Endo, M. Kurohmaru, donkey were relatively smaller than horse. All the T. Yoshihara, M. Sasaki, M. Oikawa and Y. Hayashi, anatomical structures related to the guttural pouches 2000. Macroscopic anatomy of the auditory tube resemble those in the horse with differences in the diverticulum (guttural pouch) in the thoroughbred pharyngeal recess which was deeper and larger in equine - a slicon mold approach. Okajimas Folia donkey. The volume of the guttural pouch in the males Anatomica Japonica, 76: 335-346. was more than females. 8. Sisson, S., 1975. Sisson and Grossman’s The anatomy of the domestic animals. 5th ed., W.B. REFERENCES Saunders, Philadelphia, 1: 719-727. 9. Baptiste, K.E., J.M. Naylor, J. Bailey, 1. Baptiste, K.E. and M.H. Cake, 1994. Lipid analysis of E.M. Barber, K. Post and J. Thornhill, 2000. lavage samples from the equine guttural pouch A function for guttural pouches in the horse. (auditory tube diverticulum). Annals of Otology, Nature, 403: 382-383. Rhinology and Laryngology, 103: 383-388. 10. Hodgson, D.R., 1998. What is the function of the 2. Baptiste, K.E., 1998. A preliminary study on the role guttural pouches: Selective brain cooling? of the equine guttural pouches in selective brain Augmentation of swallowing? Still to be defined. cooling. Veterinary Journal, 155: 139-148. Veterinary Journal, 155: 115-117. 3. Dyce, K.M., W.O. Sack and C.J.G. Wensing, 2002. 11. Lepage, O.M., M.F. Perron and J.L. Cadore, 2004. Textbook of Veterinary Anatomy, 3rd ed., Saunders- The mystery of fungal infection in the guttural Elsevier Science, Philadelphia, 1: 496-501. pouches. Veterinary Journal, 168: 60-64.

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