Revista Cienfica, FCV-LUZ / Vol. XXXV Recibido: 11/07/2025 Aceptado: 04/09/2025 Publicado: 13/10/2025 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 5 Revista Cienfica, FCV-LUZ / Vol. XXXV https://doi.org/10.52973/rcfcv-35748 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico Macroscopic and microscopic structure of the infraorbital sinus gland in Tuj Sheep Estudio de la estructura macroscópica y microscópica glándula del seno infraorbitario en la oveja Tuj Gülseren KirbaŞ-Doğan 1* , Ebru Karadağ-Sari 2 , Kadriye Yilmaz 2 , Şükran Yediel-Aras 3 ¹Kafkas University, Veterinary Faculty, Department of Anatomy, Kars, Turkey. ²Kafkas University, Veterinary Faculty, Department of Histology and Embryology, Kars, Turkey. ³Kaas University, Health Sciences Faculty, Department Midwifery, Kars, Turkey. ABSTRACT The infraorbital sinus (infraorbital gland-preorbital gland) is located in the lateral aspect of the skull, rostroventral to the eye, within the infraorbital fossa. Some skin glands are differenated and specialized. In the present study, it was aimed to examine the macroscopic and microscopic structure of the infraorbital sinus, which is one of these skin glands. The distance between the infraorbital foramen and infraorbital sinus was 47.35± 0.57mm on the right and 53.80±1.27 mm on the leſt. The leſt side length of the infraorbital sinus in Tuj sheep was measured as 25.32±2.21 mm, width 16.21±2.83 mm, and depth 1.23±1.80 mm. The Tuj sheep infraorbital sinus was composed of the epidermis and dermis. The epidermis was consist of keranized strafied squamous epithelium. There were many sebaceous glands, some apocrine glands, muscle fibers, and also hair follicles in the dermis. The sebaceous glands were located in the superficial region and the apocrine glands were deeper in the dermis. It was seen lots of lipid droplets inside the sebaceous gland cells. The myoepithelial cells and the basal membrane of the apocrine glands and muscle fibers were PAS-posive reacon. In conclusion, in the presented study, the macroscopic and microscopic structure of the infraorbital sinus was determined in Tuj sheep. This region is also clinically important because it is close to the infraorbital nerve passing through the infraorbital foramen (anesthesia area) and the infraorbital sinus is topographically located in this region. It is thought that it will support scienfic studies related to the skin and its appendages. Keywords: Macroscopic; microscopic; infraorbital sinus gland; Tuj sheep. RESUMEN El seno infraorbitario (glándula infraorbitaria-glándula preorbitaria) está ubicado en el aspecto lateral del cráneo, rostroventral al ojo, dentro de la fosa infraorbitaria. Algunas glándulas cutáneas están diferenciadas y especializadas. En el presente estudio, se buscó examinar la estructura macroscópica y microscópica del glándula seno infraorbitario, una de estas glándulas. La distancia entre el foramen infraorbitario y el seno infraorbitario fue de 47.35±0.57 mm en el lado derecho y de 53.80±1.27 mm en el izquierdo. La longitud del lado izquierdo del seno infraorbitario en la oveja Tuj fue de 25.32±2.21 mm, la anchura de 16.21±2.83 mm y la profundidad de 1.23±1.80 mm. El seno infraorbitario de la oveja Tuj estaba compuesto por la epidermis y la dermis. La epidermis estaba compuesta por epitelio escamoso estraficado queranizado. Se observaron numerosas glándulas sebáceas, algunas glándulas apocrinas, fibras musculares y folículos pilosos en la dermis. Las glándulas sebáceas se ubicaban en la región superficial y las apocrinas en la profundidad de la dermis. Se observaron numerosas gotas de lípidos dentro de las células de las glándulas sebáceas. Las células mioepiteliales y la membrana basal de las glándulas apocrinas y las fibras musculares dieron posivo a PAS. En conclusión, en el estudio presentado, se determinó la estructura macroscópica y microscópica del seno infraorbitario en ovejas Tuj. Esta región también es clínicamente importante porque está cerca del nervio infraorbitario que pasa por el agujero infraorbitario (área de anestesia) y el seno infraorbitario está ubicado topográficamente en esta región. Se cree que este estudio respaldará los estudios cienficos relacionados con la piel y sus apéndices. Palabras clave: Macroscópica; microscópica; glándula del seno infraorbitario; oveja Tuj. Correspondence author: glsrn36@gmail.com
Macroscopic and microscopic structure of the Infraorbital sinus gland / Kirba�-Doğan et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION In addion to being a sense organ, the skin also has dues such as protecng the body, providing temperature regulaon, and removing toxic substances. Integumentum communae is a comprehensive organ that covers structures such as subcutaneous connecve ssue, dermis, epidermis, hairs, nails, horns, mammary glands, and skin glands [1 ,[2]. The skin glands differ between species in size, shape, and locaon. Some are differenated and specialized and are associated with sacs in the skin [3]. One of these glands, the infraorbital sinus (infraorbital gland-preorbital gland), is located in a skin sac in the rostral of the eye. In sheep (Ovis aries), they open to the ventrolateral of the face. The wall of the gland contains sebaceous and serous glands that stain the skin when secreons come out of the gland. These glands, which are responsible for marking their habitat, are larger in rams [4]. Reproducve communicaon in ungulates is thought to be via the infraorbital sinus, interdigital sinus, and tarsal glands, which are skin glands associated with many scents [5]. The presence of infraorbital sinus gland has been reported in sheep, goats, deer, and antelopes [6 , 7]. This gland and the external lacrimal fossa in which the gland is located varies according to the animal species. External lacrimal fossa is an important anatomical structure to disnguish sheep and goat heads. This structure is found in sheep but not in goats [8]. The region where the infraorbital sinus gland is located is also important because it is close to the infraorbital foramen. The infraorbital nerve, which is the connuaon of the maxillar nerve from the infraorbital foramen, leaves the head [3] Aſter exing the infraorbital nerve infraorbital foramen; it ends by dividing into three branches that disperse on the lateral surface of the nose, the dorsal surface of the nose, and the upper lip skin [8]. The infraorbital sinus is lined by thin skin and is composed of modified sebaceous and apocrine glands. The secreons of these glands are responsible for the scky, yellow fay substance on the skin [9]. There are studies on infraorbital sinus gland in some animal species [10 , 11 , 12]. However, in the literature review, no study was found on the infraorbital sinus gland in Tuj sheep. In the presented study, informaon was given about the macroscopic and microscopic structure of the infraorital sinus gland in Tuj sheep. MATERIAL AND METHODS Anatomical procedures In the presented study, skulls of 5 male and 5 female Tuj sheep around 2 years old were used. Tuj sheep heads supplied as slaughterhouse material were preserved in 10% formaldehyde soluon. Infraorbital sinus was exposed by disseconand with a digital calliper the morphometric measurements were made (Stainless 0-150 mm, 0.00, BTS, UK). Materials were photographed with Canon digital camera zoom lens 5X. 17. The measured morphometric values were evaluated in the SPSS 20 program. For the use of scienfic terms N.A.V. [12] was applied. Aſter the anatomical findings were obtained, the histological procedure was performed. Histological procedures The infraorbital sinus gland was fixed in 10% formalin for 24 h, dehydrated, cleared, and embedded in paraffin. The 5 µm thick serial secons were cut and stained with Mallory’s modified triple stain to demonstrate general structure of the infraorbital sinus. For glycogen demonstraon Periodic Acid Schiff (PAS) stain was applied to the secons. The secons were examined under light microscope (Zeiss Primostar 3, Germany). RESULTS AND DISCUSSION Anatomical results and discussion In Tuj sheep, it was observed that the infraorbital sinus gland was located in the external lacrimal fossa on the lacrimal bone, just adjacent to the ocular angular vein, above the inial tendon of the malar muscle (FIG. 1). It was determined that the infraorbital sinus was in the form of a plump circle. Aſter removing this gland, the external lacrimal fossa was found to be clearly idenfiable (FIG. 2). It was determined that the distance between the infraorbital sinus gland and the infraorbital foramen in one animal material was greater than in other substances. The distance between the infraorbital foramen and infraorbital sinus was taken as shown in FIG. 3. FIGURE 1. Infraorbital sinus gland and nearby anatomical structures in male Tuj sheep head (a: infraorbital sinus, b: nasal dorsal vein, c: zygomac muscle, d: superior labial vein, e: malar muscle). The distance between the infraorbital foramen and infraorbital sinus gland was 42.23±1.22 mm on the right side in females, 46.71±1.82 mm on the leſt in females, 47.35±0.57 mm on the right side in males and 53.80±1.27 mm on the leſt in males. The leſt side length of the infraorbital sinus gland in female Tuj sheep was measured as 25.32±2.21 mm, width 16.21 ± 2.83 mm, and depth 1.23±1.80 mm. The length of the 2 of 5
Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico infraorbital sinus gland on the right side in female Tuj sheep was measured as 24.51±1.81 mm, width 14.52±1.33 mm, and depth 1.19±2.44 mm. The leſt side length of the infraorbital sinus gland in male Tuj sheep was 28.11±1.51 mm, width was 18.31±2.63 mm, and depth was 1.62±3.33 mm. In male Tuj sheep, the length of the infraorbital sinus gland on the right side was 27.01±2.33 mm, width was 17.22±1.62 mm, and depth was 1.29±2.13 mm. In general, looking at the measurement results, it can say that the leſt side parameters are higher than the right side in female and male Tuj sheep. The measured parameters are related to the size of the gland. An organ’s growth may be related to the amount of oxygenated blood it receives, but it is not the sole criterion. The altude at which the animal lives may also have an impact on the development of the organ. Normally, the anatomical structures on the right and leſt sides of the body are similar in size. However, the artery supplying one side may be larger than the other, or the increased blood volume may have caused the artery to receive more blood and enlarge. Therefore, it is thought that the artery supplying the leſt infraorbital sinus may be larger [13]. FIGURE 2. External lacrimal fossa and infraorbital nerve in head of Tuj sheep (red circle: external lacrimal fossa, green circle: infraorbital nerve). FIGURE 3. Distance between infraorbital foramen and infraorbital sinus gland in female Tuj sheep. Infraorbital sinus gland was found to be bean-shaped [7] in male antelopes and pear-shaped in Nave Egypan sheep [5]. It was in the shape of a plump circle in Tuj sheep. In antelopes, infraorbital sinus gland length has been reported to be 28-35 mm, wide 15-17 mm, deep 1-1.2 mm [7]. In male nave Egypan sheep, this gland is 28-33 mm length, 25-28 mm width, 3-5 mm depth. It has been reported that females are 24-27 mm in length, 20-22 mm in width, and 2-4 mm in depth [5]. In male Tuj sheep, this gland was 27-28 mm length, 17-18 mm width, 1-1.5 mm depth. It has been measured in male Munchaks (barking deer) 23-27 mm length and 20-30 mm width [14]. In general, the measurement results were found to be closer to the results of Rajagopal and Archunan [7] in terms of all parameters. In terms of length, it was close to the Munchaks [14]. It was 24-25 mm length, 14-16 mm width, 1-2.5 mm depth in female Tuj sheep. The length of the infraorbital sinus gland was close to Moawad [5] when compared in females, while other parameters differed. The Tuj sheep infraorbital sinus gland was composed of the epidermis and dermis. The epidermis was consist of keranized strafied squamous epithelium. There were many sebaceous glands, some apocrine glands, muscle fibers, and also hair follicles in the dermis. The sebaceous glands were located in the superficial region and the apocrine glands were deeper in the dermis. It was seen lots of lipid droplets inside the sebaceous gland cells (FIG. 4, 5, 6). The myoepithelial cells and the basal membrane of the apocrine glands and muscle fibers were PAS- posive reacon (FIGS. 7, 8, 9). FIGURE 4. Male Tuj sheep infraorbital sinus gland. e: epidermis, d: dermis, s: sebaceous glands, a: apocrine glands, and h: hair follicles. Mallory’s modified triple stain. Scale bar: 500 μm FIGURE 5. Male Tuj sheep infraorbital sinus gland. a: apocrine glands. Mallory’s modified triple stain. Scale bar: 100 μm 3 of 5
Macroscopic and microscopic structure of the Infraorbital sinus gland / Kirba�-Doğan et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico FIGURE 6. Male Tuj sheep infraorbital sinus gland. s: sebaceous glands. Mallory’s modified triple stain. Scale bar: 50 μm Infraorbital sinus gland is thought to have other funcons in addion to its role in marking [15]. It has been reported that deer open these infraorbital sinus gland while fighng [16]. Hatlapa [17] showed that preorbital secreons in red deer have a primary funcon in establishing mother-offspring bonds. It is also reported that the opening of the infraorbital sinus gland in fallow deer offspring is a signal to the mother that the calf is hungry [18 ,[19]. When look at the results of the study, it is beer understand the importance of infraorbital sinus gland in providing communicaon. FIGURE 7. Male Tuj sheep infraorbital sinus gland. PAS (+) reacon. m: muscle fiber. PAS stain. Scale bar: 100 μm FIGURE 8. Male Tuj sheep infraorbital sinus gland. PAS (+) reacon. arrow: myoepithelial cells. PAS stain. Scale bar: 50 μm FIGURE 9. Male Tuj sheep infraorbital sinus gland. PAS (+) reacon. m: muscle fibers. PAS stain. Scale bar: 50 μm The infraorbital sinus gland with large air spaces are in pairs, facing the nasal cavity, and lined with respiratory epithelium. It is located medial and rostal of the eye in sheep and covered with a thin skin with few hairs. It has sebaceous glands that form a connuous layer around it and several peripherally located apocrine sweat glands. The secreons of these glands are responsible for the formaon of the scky yellow oily substance in the skin [20]. There have been reports about the infraorbital sinus gland of Formosan serow [10], Steenbok [21], barking deer [14], blackbuck Antelope cervicapra [7] and Egypan nave breed sheeps [5] but not Tuj sheep. It was determined that the infraorbital sinus gland had two glandular components: one sebaceous secretory units and the other apocrine secretory units. These glands were surrounded by connecve ssue and muscle fibers [7]. It has been suggested striated muscle fibers pass up between the sebaceous glands to the connecve ssue of the stratum papillare and the contracon of these muscles should force the secreon out as small black granules in steenbok infraorbital sinus gland. It has also reported that these muscles could be strands from either the nasolabial levator muscle, malar muscle or both [21]. The Tuj sheep infraorbital sinus gland was composed of the epidermis and dermis. The epidermis was consist of keranized strafied squamous epithelium. There were many sebaceous glands, some apocrine glands, muscle fibers, and also hair follicles in the dermis. It has stated that apocrine glands was larger than the sebaceous glands in infraorbital sinus gland of barking deer [14] but in the study it was seen that sebaceous glands are larger than apocrine glands. The sebaceous glands were located in the superficial region and the apocrine glands were deeper in the dermis. It was seen lots of lipid droplets inside the sebaceous gland cells in infraorbital sinus gland of Tuj sheep like steenbok infraorbital sinus gland [22]. Moawad [5] has suggested that the only apocrine acini reacted posively with the Periodic acid shiff stain in Egypan nave breed sheeps infraorbital sinus gland how ever in the study demonstrated that the myoepithelial cells and the basal membrane of the apocrine glands and muscle fibers were PAS- posive reacon in Tuj sheep infraorbital sinüs gland. CONCLUSIONS As a result, the infraorbital sinus gland is important because it is close to the infraorbital foramen apart from its role in communicaon between animals. Infraorbital nerve passes through this opening. The topographic locaon of the infraorbital sinus gland can assist in the selecon of the 4 of 5
Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico anesthesia site when performing regional anesthesia. In this sense, measurement values become even more important. It is thought that this study will contribute to the macroscopic, microscopic, and surgical operaons to be performed in the infraorbital region. Conflict of interest The authors declared that there is no conflict of interest. Data availability statement The data supporng this study’s findings are available from the corresponding author upon reasonable request. Ethical statement To conduct this study, necessary permissions were first ob- tained from Kaas University Animal Experiments Local Ethics Commiee (KAU-HADYEK/2023-082). BIBLIOGRAPHIC REFERENCES [1] Demiraslan Y, Orhun-Dayan M. Veteriner Sistemak Anatomi. 1st. ed. Ankara, Turkey: Atlas Kitabevi; 2021. [2] Demiraslan Y, Orhun-Dayan M. VETKA-Veteriner Klinik Anatomi. 1st. ed.Ankara, Turkey: Nobel Akademik Yayincilik; 2023. [3] König HE, Liebich HG. Veteriner Anatomi (Evcil Memeli Hayvanlar). 3rd. ed.Turkey: Medipres; 2022. [4] Haziroglu RM, Cakir A, editors. Veteriner Anatomi Konu Anlamı ve Atlas. 4th. ed. Ankara: Güneş Tip Kitabevleri; 2017. [5] Moawad UK. Morphological, histochemical and morphometric studies of the preorbital gland of adult male and female egypan nave breeds of sheep (Ovis aries).Asian J. Anim. Vet. Adv. [Internet]. 2016; 11(12):771-782. doi: hps://doi.org/p73r. [6] King N, Kumar AHS, Kilroy D. Ovine infraorbital (preorbital) pouch: an unusual presentaon in a male lamb.Biol. Eng. Med. Sci. Rep. [Internet]. 2018; 4(1):01-02. doi: hps:// doi.org/p73s. [7] Rajagopal T, Archunan G. Histomorphology of preorbital gland in territorial and non-territorial male blackbuck Antelope cervicapra, a crically endangered species.Biol. [Internet]. 2011; 66:370-378. doi: hps://doi.org/cj22wj. [8] Dursun N. Veteriner Anatomi II. 12th. ed. Ankara: MedisanPublishing House; 2008. [9] Delmann HD, Brown EM. Textbook of Veterinary Histology. 2nd. Ed. Philapelphia: Lea & Febiger; 1981. [10] Atoji Y, Yamamoto Y, Suzuki Y. Infraorbital glands of a male formosan serow (Capricornis crispus swinhoei). Eur. J. Morphol. [Internet]. 1996; 34(2):87-94. doi: hps:// doi.org/fpczwb. [11] Ceaceroa F, Pluhácek J, Komárková M, Zábranský M. Pre- orbital gland opening during aggressive interacons in Rusa deer (Rusa morensis). Behav. Proces. [Internet]. 2015; 111:51–54. doi: hps://doi.org/f62ppw. [12] N.A.V. Internaonal Commiee on Veterinary Gross Anatomical Nomenclature. Nomina Anatomica Veterinaria (I.C.V.G.A.N.). 6th. ed. World Associaon of Veterinary Anatomists: Hanover (Germany), Ghent (Belgium), Columbia, MO (U.S.A.), Rio de Janeiro (Brazil); 2017. [13] Liu M, Yang Y, Li M, Cai Y, Zhao S, Wang X. Comparison study of morphology andvascular casts between plateau- type Tibetan sheep andlow-altude small-tailed Han sheep testes. Anat. Histol. Embryol. [Internet]. 2022; 51(4):524–532. doi: hps://doi.org/p74r. [14] Adnyane IKM, Zuki ABZ, Noordin MM, Wahyuni S, Agungpriyono S. Morphological study of the infraorbital gland of the male barking deer, munacus muntjak. Afr. J. Biotechnol. [Internet]. 2011; 10(77):17891-17897. Available in: hps://goo.su/TOR4k. [15] Cluon-Brock T, Guinness FE, Albon SD. Red Deer, Behaviour and Ecology of Two Sexes. 1st. ed. Chicago, IL: University of Chicago Press; 1982. [16] Bartos L. Some observaons on the relaonship between preorbital gland opening and social interacons in red deer. Aggress. Behav. [Internet]. 1983; 9(1):59–67. doi: hps://doi.org/dvpzk2. [17] Hatlapa HH. Zur biologischen Bedeutung des praorbital Organs beim Rotwild, Pragung, Individualgeruch, Orienerung. Berl. Munch. Tierartzl. Wochenschr. 1977; 90:100–104. [18] Wolfel H. Zur Jugendentwicklung, Muer-Kind-Bindung und Feindvermeidung beim Rothirsch (Cervus elaphus) II. Z. Jagdwissensch. [Internet]. 1983; 29:197–213. doi: hps://doi.org/dgdq8t. [19] Bartos L, Víchová J, Lancingerová J. Preorbital gland opening in red deer (Cervus elaphus) calves: Signals of hunger?. J. Anim. Sci. [Internet]. 2005; 83(1):124–129. doi: hps://doi.org/p746. [20] Eurell JA, Frappier BL. Dellmann’s Textbook of Veterinary Histology. 6th. ed. Iowa (USA), Oxford (UK): Blackwell Publishing; 2006. [21] Gernek WH, Cohen M. The micromorphology of the glands of the infra-orbital cutaneous sinus of the Steenbok (Raphıcerus Campestrıs). Onderstepoort J. Vet. Res. [Internet]. 1978; 45(2):59-66. [22] Mohamed R, Driscoll M, Mootoo N. Clinical anatomy of the skull of the Barbados Black Belly sheep in Trinidad. Int. J. Curr. Res. Med. Sci. [Internet]. 2016; 2(8):8-19. Available in: hps://goo.su/fQ9X. 5 of 5