Abstract
Normal structure of the accessory organs of the eye is essential for normal eye physiology. Among the most important accessory organs of the eye are the eyelids, the conjunctiva-associated lymphoid tissue (CALT) and the lacrimal gland (LG). The aim of this study was to demonstrate the histological structure of the eyelids and LG by histochemical and ultrastructural analysis. The study was performed on 13 adult female Bilgorajska geese. Eyelid samples were stained with the Alcian blue (AB pH 2.5) and periodic acid-Schiff (PAS) methods. Staining methods used for LG were AB pH 2.5, aldehyde fuchsin (AF), PAS and Hale’s dialysed iron (HDI). Within the connective tissue of the eyelids, well-developed, diffuse, CALT follicles were observed, mostly under the conjunctival epithelium. Numerous lymphocytes were present within loose connective tissue. Staining of the eyelids with the PAS method demonstrated the presence of goblet cells of a mucous nature, and AB pH 2.5 staining indicated the presence of sulfated acid mucopolysaccharides. PAS staining of LG revealed the presence of secretory cells containing weakly PAS-positive granules. All epithelial cells of the corpus glandulae and the duct systems reacted positively to AB pH 2.5. HDI staining detected the presence of carboxylated acid mucopolysaccharides. Transmission electron microscopy investigations revealed two types of secretory epithelial cells in LG. Both types of LG cells contained drop-like secretory vesicles of different sizes with low or high electron density in cytoplasm, as well as small and large lipid vacuoles, and numerous small primary lysosomes.
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Aşti RN, Kurtdede N, Altunay H, Ozen A (2000) Electron microscopic studies on conjunctiva associated lymphoid tissue (CALT) in Angora goats. Dtsch Tierarztl Wochenschr 107:196–198
Astley RA, Kennedy RC, Chodosh J (2003) Structural and cellular architecture of conjunctival lymphoid follicles in the baboon (Papioanubis). Exp Eye Res 76:685–694
Baumel JJ (ed) (1993) Handbook of avian anatomy: Nomina Anatomica Avium, 2nd edn. Harvard Univ Nuttall Ornithological Club, Cambridge, MA
Bayraktaroglu AG, Aşti RN (2009) Light and electron microscopic studies on Conjunctiva Associated Lymphoid Tissue (CALT) in cattle. Revue Med Vet 160:252–257
Bayraktaroglu AG, Kormaz D, Aşti RN, Kurtdede N, Altunay H (2011) Conjunctiva associated lymphoid tissue in the ostrich (Struthio camelus). Kafkas Univ Vet Fak Derg 17:89–94
Burns RB (1979) Histological and immunological studies on the fowl lacrimal gland following surgical excision of Harder’s gland. Res Vet Sci 27:69–75
Burns RB (1992) The Harderian gland in birds: histology and immunology. In: Webb SM, Hoffman RA, Puig-Domingo ML, Reiter RJ (eds) Harderian glands: porphyrin metabolism, behavioral and endocrine effects. Springer, Berlin, pp 155–163
Burns RB, Maxwell MH (1979) The structure of the Harderian gland and lacrimal gland ducts of the turkey, fowl and duck. A light microscope study. J Anat 128:285–292
Cain C, Phillips TE (2008) Developmental changes in conjunctiva-associated lymphoid tissue of the rabbit. Invest Ophthalmol Vis Sci 49:644–649
Cesta MF (2006) Normal structure, function and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 34:599–608
Chieffi Baccari G, Minucci S, Di Matteo L, Chieffi G (1990) Harderian gland and the lacrimal gland of the lizard Podarcis s. sicula: histology, histochemistry, and ultrastructure. Anat Rec 226:269–278
Chieffi Baccari G, Di Matteo L, Minucci S (1992) The orbital glands of the chelonians Pseudemys scripta and Testudo graeca: comparative histological, histochemical and ultrastructural investigations. J Anat 180:1–13
Chieffi Baccari G, Di Matteo L, Minucci S (1995) Organogenesis of the orbital glands in the lizard Podarcis s. sicula: a histological, histochemical and ultrastructural study. Anat Embryol 192:43–52
Chodosh J, Nordquist RE, Kennedy RC (1998) Anatomy of mammalian conjunctival lymphoepithelium. Adv Exp Med Biol 438:557–565
Dartt DA (2009) Neural regulation of lacrimal gland secretory processes: relevance in dry eye diseases. Prog Retin Eye Res 28:155–177
Dimitrov D (2011) Intraorbital glands in turkey broilers. Lacrimal gland histometry. J Agric Sci Technol 3:327–329
Dimitrov DS, Nikiforov IP (2005) Histological and histochemical studies of Harderian gland, lacrimal gland and bursa of fabricius in mallard ducks (Anas sterilis) with chlamydial infection. Bulg J Vet Med 8:119–127
Fix AS, Arp LH (1989) Conjunctiva-associated lymphoid tissue (CALT) in normal and Bordetella avium-infected turkeys. Vet Pathol 26:222–230
Fix AS, Arp LH (1991) Particle uptake by conjunctiva-associated lymphoid tissue (CALT) in turkeys. Avian Dis 35:100–106
Flanagan JL, Willcox MD (2009) Role of lactoferrin in the tear film. Biochimie 91:35–43
Franklin RM, Remus LE (1984) Conjunctival-associated lymphoid tissue: evidence for a role in the secretory immune system. Invest Ophthalmol Vis Sci 25:181–187
Freeman BM (1965) The importance of glycogen at the termination of the embryonic existence of Gallus domesticus. Comp Biochem Physiol 14:217–222
Funaki C, Hodges RR, Dartt DA (2010) Identification of the Raf-1 signaling pathway used by cAMP to Inhibit p42/p44 MAPK in rat lacrimal gland acini: role in potentiation of protein secretion. Invest Ophthalmol Vis Sci 51:6321–6328
Gargiulo AM, Coliolo P, Ceccarelli P, Pedini V (1999) Ultrastructural study of sheep lacrimal gland. Vet Res 30:345–351
Harris MC, Schorling JJ, Herring IP, Elvinger F, Bright PR, Pickett JP (2008) Ophthalmic examination findings in a colony of Screech owls (Mega scopsasio). Vet Ophthalmol 11:186–192
Jezler PCO, Braga MBP, Perlmann E, Squarzoni R, Borella MI, Barros PSM, Milanelo L, Antunes A (2010) Histological analysis of the eyeballs of the striped owl Rhinoptynxclamator. In: Méndez-Vilas A, Díaz J (eds) Microscopy: science, technology, applications and education. Formatex, Madrid, pp 1047–1054
Jones MP, Pierce KE, Ward DW (2007) Avian vision: a review of form and function with special consideration to birds of prey. J Exotic Pet Med 16:69–87
Jordan D (1990) Accessory lacrimal glands. Ophthalmol Surg 2:146–147
Kageyama M, Nakatsuka K, Yamaguchi T, Owen RL, Shimada T (2006) Ocular defense mechanisms with special reference to the demonstration and functional morphology of the conjunctiva-associated lymphoid tissue in Japanese monkeys. Arch Histol Cytol 69:311–322
Kawashima M, Kawakita T, Inaba T, Okada N, Ito M, Shimmura S, Watanabe M, Shinmura K, Tsubota K (2012) Dietary lactoferrin alleviates age-related lacrimal gland dysfunction in mice. PLoS One 7:e33148
Kern TJ (2007) Exotic animal ophthalmology. In: Gelatt KN (ed) Veterinary ophthalmology, 4th edn. Blackwell, Oxford
Klećkowska-Nawrot J, Dzięgiel P (2008) Morphology of lacrimal gland in pig fetuses. Anat Histol Embryol 37:74–77
Klećkowska-Nawrot J, Marycz K, Czogała J, Kujawa K, Janeczek M, Chrószcz A, Brudnicki W (2013) Morphology of the lacrimal gland and superficial gland of the third eyelid of Roe deer (Capreolus capreolus L.). Pak Vet J 2:139–144
Knop N, Knop E (2000) Conjunctiva-associated lymphoid tissue in the Human Eye. IOVS 41:1270–1279
Kraehenbuhl JP, Neutra MR (1992) Molecular and cellular basis of immune protection of mucosal surfaces. Physiol Rev 72:853–879
Książkiewicz J (2006) The role and importance of geese species included by genetic stock protection program. Wiadomosci Zootechniczne 4:34–38
Lavach JD (1990) Large animal ophthalmology, vol 1. Mosby, St Louis
Martin CL, Munnell J, Kaswan R (1988) Normal ultrastructure and histochemical characteristics of canine lacrimal glands. Am J Vet Res 49:1566–1572
Maxwell MH, Rothwell B, Burns RB (1986) A fine structural study of the turkey Harderian gland. J Anat 148:147–157
Mestecky J (1987) The common mucosal immune system and current strategies for induction of immune responses in experimental secretions. J Clin Immunol 7:265–276
Mohammadpour AA (2008) Anatomical characteristics of dorsal lacrimal gland in one humped camel (Camelus dromedarius). J Biol Sci 8:1104–1106
Mohammadpour AA (2009) Morphological and histological study of superior lacrimal gland of third eyelid in camel (Camelus dromedarius). Iran J Vet Res 10:334–338
Mohammadpour AA (2011) Histochemistry of dorsal lacrimal gland in camel (Camelus dromedarius). J Camel Pract Res 18:131–133
Pabst R, Westermann J (1994) Which steps in lymphocyte recirculation are regulated by interferon-gamma? Res Immunol 145:289–294
Payne AP (1994) The Harderian gland: a tercentennial review. J Anat 185:1–49
Pinard CL, Weiss ML, Brightman AH, Fenwick BW, Davidson HJ (2003) Normal anatomical and histochemical characteristics of the lacrimal glands in the american bison and cattle. Anat Histol Embryol 32:257–262
Reese AM (1925) The cephalic glands of Alligator mississippiensis, Florida alligator and of Agkistrodon, copperhead and moccasin. Biol Gend 1:482–500
Rehorek SJ, Legenzoff EJ, Carmody K, Smith TD, Sedlmayr JC (2005) Alligator tears: a reevaluation of the lacrimal apparatus of the crocodilians. J Morphol 266:298–308
Romanov MN (1999) Goose production efficiency as influenced by genotype, nutrition and production systems. World Poult Sci Assoc 9:281–294
Rothwell B, Wight PAL, Burns RB, MacKenzie GM (1972) The Harderian glands of the domestic fowl III. Ultrastructure. J Anat 112:233–250
Saint-Girons H (1985) Histologie des glandes orbitaires des Crocodiles et des Tortues et comparaison avec les Lepidosauriens. Ann Sci Nat Zool Paris 7:249–264
Sakai T (1989) Major ocular glands (harderian gland and lacrimal gland) of the musk shrew (Suncus murinus) with a review on the comparative anatomy and histology of the mammalian lacrimal glands. J Morphol 201:39–57
Schechter JE, Warren DW, Mircheff AK (2010) A lacrimal gland is a lacrimal gland, but rodent’s and rabbit’s are not human. Ocul Surf 8:111–134
Scherf BD (ed) (2000) World watch list for domestic animal diversity, 3rd edn. Food and Agriculture Organization of the United Nations, Rome
Spicer SC, Henson JG (1967) Methods for localizing mucosubstances in epithelial and connective tissue. In: Bajusz E, Jamin F (eds) Series on methods and achievements in experimental pathology, vol 2. Karger, Basel
Steven P, Gebert A (2009) Conjunctiva-associated lymphoid tissue- current knowledge, animal models and experimental prospects. Ophtalmic Res 42:2–8
Van Ginkel FW, Gulley SL, Lammers A, Hoerr FJ, Gurjar R, Toro H (2012) Conjunctiva-associated lymphoid tissue in avian mucosal immunity. Dev Comp Immunol 36:289–297
Waibl H, Gasse H, Constantinescu G, Hashimoto Y, Simoens P (2012) Nomina anatomica veterinaria, 5th edn, revised version. Gasse H, Van Den Broeck W, Hashimoto Y, Constantinescu G, Budras K-D, Saber A, Simoens P et al (eds). Hannover, Germany; Columbia, MO; Ghent, Belgium: Editorial Committee, available at: http://hdl.handle.net/1854/LU-3147919
Wight PAL, MacKenzie GM, Rothwell B, Burns RB (1971) The Harderian gland of the domestic fowl II. Histochemistry. J Anat 110:323–333
Wolf JL, Bye WA (1984) The membranous epithelial (M) cell and the mucosal immune system. Annu Rev Med 35:95–112
Zagon IS, Campbell AM, Sassani JW, McLaughlin PJ (2012) Spontaneous episodic decreased tear secretion in rats is related to opioidergic signaling pathways. Invest Ophthalmol Vis Sci 53:3234–3240
Zawistowski S (1965) Technika histologiczna oraz podstawy histopatologii. PZWL
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This research was supported by statutory research and development activity funds assigned to Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences.
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Klećkowska-Nawrot, J., Nowaczyk, R., Goździewska-Harłajczuk, K. et al. Light and electron microscopic study of the eyelids, conjunctiva-associated lymphoid tissue and lacrimal gland in Bilgorajska Goose (Anser anser). Anat Sci Int 91, 74–88 (2016). https://doi.org/10.1007/s12565-015-0274-1
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DOI: https://doi.org/10.1007/s12565-015-0274-1