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Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.19 n.1 Temuco abr. 2001

http://dx.doi.org/10.4067/S0716-98682001000100010 

MORPHOLOGY OF THE SUBMANDIBULAR GLAND OF THE GERBIL
(Meriones unguiculatus). A MACROSCOPIC AND LIGHT MICROSCOPY STUDY

MORFOLOGÍA DE LA GLÁNDULA SUBMANDIBULAR DEL GERBIL (Meriones
unguiculatus
). ESTUDIOS MACROSCÓPICO Y MICROSCÓPICO

Bazan, E.*; Watanabe, I.**; Iyomasa, M. M.***; Mizusaki, C. I.***; Sala, M.*** & Lopes, R. A.***

SUMMARY: The morphology of the submandibular gland of the gerbil was studied using macroscopic and microscopic techniques. Ten gerbils were anesthetized and perfused with 10% formalin and the anterior cervical region of each animal was dissected for macroscopic analysis of the submandibular gland. For histological analysis, the pieces were fixed in the same solution and embedded in paraffin for routine processing. Serial 6-mm thick sections were stained with hematoxylin-eosin and picrosirius for light microscopy analysis. The results showed that the submandibular gland of the gerbil is ovoid in shape and is located in the submandibular region, measuring about 9.0 mm in length and 5.9 mm in width. Histologically, the acini consist of four irregularly arranged cell types. The ductal system consists of four distinct segments, i.e., intercalary duct, granulose duct, striated duct, and excretory duct, each with different characteristics.

KEY WORDS: 1. Submandibular gland; 2. Morphology; 3. Acini and ducts; 4. Connective tissue; 5. Gerbil- Meriones unguiculatus.

INTRODUCTION

The morphofunctional knowledge of the submandibular gland of various animals is of fundamental importance for structural comparison and also as a contribution to the diagnosis of certain types of systemic or metabolic diseases. An understanding of the salivary glands within the context of diet, dentition and behavior can also lead to a better understanding of animal adaptation (Phillips & Tandler, 1996).

The morphological structure of the submandibular gland has been studied in rodents, rats mice and rabbits (Tamarin & Sreebny, 1965; Espinal et al., 1983; Shimono et al., 1992; Watanabe et al., 1992; 1996; 1997). Although the gerbil is a rodent widely used in laboratory studies mainly related to the vascular and nervous system, few morphological and angioarchitectural descriptions of its salivary glands are available. Thus, the objective of the present report was to describe the morphology of the submandibular gland of the gerbil (Meriones unguiculatus).

MATERIAL AND METHOD

Ten adult male gerbils (Meriones unguiculatus) were used. For the macroscopic study, five animals were anesthetized with sodium pentobarbital and intracardially perfused with 10% formalin in sodium phosphate buffer, pH 7.4. The submandibular region was dissected for analysis of the macroscopic gland characteristics, i.e., topographic localization, size and shape, and their relations with the sublingual gland. For the light microscopy study the submandibular glands of 5 animals were removed an immersed in the fixative solution mentioned above. The material was then dehydrated in a growing alcohol series and routinely processed for paraffin embedding. Six-µm thick transverse sections were obtained and stained with hematoxylin-eosin and picrosirius for light microscopy.

RESULTS

The submandibular glands of the gerbil are ovoid in shape, about 9.0 mm in length and 5.9 mm in width and located on the ventral surface of the neck. They are related to the subcutaneous network and skin superficially, to the anterior portion of the posterior belly of the digastric muscle deeply, to the anterior belly of the digastric muscle and lymph nodes cranially, and to brown fat and sternocleidomastoid muscle caudally. Laterally, the gland is related to the parotid gland and masseter muscle close to the mandibular angle, and medially to some lymph nodes. The sublingual gland, intimately related to the submandibular gland, is located superolaterally to the latter (Fig. 1. A).


Fig. 1. A) General view of the submandibular region of the gerbil (Meriones unguiculatus). Observe the submandibular gland (*) associated with the sublingual gland (**) delimited inferiorly by brown fat (arrow) and superiorly by the anterior belly of the digastric muscle (curved arrow). 5X. B) Submandibular gland of the gerbil. The figure shows the general aspect of the connective tissue capsule (curved arrow), acinar portion (arrow), and granulose duct portion (*). HE. 40X. C) The figure shows the acinar shape of the secretory portion and of Type I (*), II (arrowhead), III (arrow), and IV (curved arrow) cells. HE. 400X.

 

Light microscopy revealed that the gland is enveloped by a capsule of connective tissue superficially fibrous and slightly loose in the deep layers close to the glandular parenchyma (Fig. 1. B). Septa of this connective tissue divide the gland into lobes and lobules. The secretory portion is of the acinous type, of slightly irregular aspect (Fig. 1. C), with no half-moon formations and consisting of different cell types, as shown in Table I.

Table I. Cells composing the secretory portion of the submandibular gland.
Cell
Shape
Nucleus
Cytoplasm
Localization
Type I Pyramidal Flattened Large vesicles in the apical pole Secretory portion
Type II Pyramidal Spherical or elliptical Small vesicles, basophilic Secretory portion
Type III Pyramidal Spherical or Flattened Small and large, light vesicles
at the apical pole
Secretory portion
Type IV Pavement-like Flattened Basophilic On the basal surface of Type I and II cells

The ductal system presented four segments: intercalary duct, granulose duct, striated duct, and excretory duct. The intercalary duct is of small diameter when observed transversely and consists of pavement-like cells with an intensely stained central nucleus and scarce and light cyctoplasm close to the nucleus and more eosinophilic and granulose at the periphery (Fig. 2. A). The granulose duct, present in large numbers in the gland, consists of four cell types, as shown in Table II.

Fig.2. A) Intercalary (curved arrow) and granulose ducts (arrow) ducts. HE. 400X.

Table II. Cells composing the granulose duct of the submandibular gland.
Cell
Shape
Nucleus
Cytoplasm
Localization
Type I Cylindric Pavement-like and light Eosinophilic granules Forming the wall of the duct
Type II Cylindric Pavement-like and dark Scarce and basophilic Forming the wall of the duct
Type III Cylindric Voluminous and light With large vacuoles and basophilic Forming the wall of the duct
Type IV Pavement-like Flattened (pavement-like) Basophilic Basal surface of ductal cells
         

The striated duct (Fig. 2. B) consists of tall cuboidal and cylindric cells, whose characteristics are described in Table III.

B) Observe the nuclei and the acinar structures adjacent to the striated duct (arrow). HE. 400X.

Table III. Cells composing the striated duct of the submandibular salivary gland.
Cell
Shape
Nucleus
Cytoplasm
Localization
Type I Cuboidal or cylindric Central and dark Acidophilic and striated in the basal pole Forming the wall of the duct
Type II Cuboidal or cylindric Central and light Granulose and light Forming the wall of the duct

The excretory duct (Fig. 2. C), consisting of pseudostratified cylindric epithelium, presented three different cell types, as shown in Table IV.

C) Segment of the excretory duct showing Type I (curved arrow), II (arrow) and III (arrowhead) cells. HE. 400X.

Table IV. Cells that compose the excretory duct of the submandibular gland.
Cell Shape Nucleus Cytoplasm Localization
Type I Cylindric or cuboidal Spherical and light Basophilic Forming the wall of the duct
Type II Pyramidal and small Pavement-like and dark Scarce and acidophilic Forming the wall of the duct
Type III Cylindric Spherical and dark With granulation and acidophilic Forming the wall of the duct

The stroma of the salivary gland is quite scarce, but a large quantity of capillaries are observed near the granulose and striated ducts. Large amounts of reticular fibers supporting the secretory portion and duct belonging to the basement membrane were observed (Fig. 2. D). Collagen fibers in large numbers were detected by polarized light, mainly located in the capsule and septa and supporting the vessels and ducts (Fig. 2 E).

D) Basement membrane (arrow) consisting of collagen fibers of the acinar and excretory portion. Picrosirius. 400X.

E) The figure shows the connective tissue capsule (curved arrow) and septa between the lobules (arrow). Picrosirius and Polarized light microscopy. 40X.

DISCUSSION

The submandibular gland of the gerbil was found to be morphologically similar to the descriptions for rodents made by Greene (1959), but differed from human salivary glands. The secretory unit of the gerbil has irregular acini with no half-moon formation and consisting of four cell types irregularly arranged inside the secretory portion. These structures are present in the tubular-acinar shape in bats (Pinkstaff et al., 1982) and in other rodents (Espinal et al.; Watanabe et al., 1992., 1996, 1997).

The secretory portion is normally described as having mucosal and serosal cells, the latter being called seromucosal cells. Ultrastructural studies of the acinar cells of rodents have shown secretion granules of varying diameters (Watanabe et al., 1992, 1996, 1997; Bezerra et al., 1999), with the Golgi apparatus located close to the nucleus and the rugose endoplasmic reticulum located in the basal portion among the mitochondria. The light perinuclear area observed in type I and type II cells in the present study seems to correspond to the Golgi complex region described by the cited authors. Nagato et al. (1998) reported a seromucosal cell type with granules clearly differing from those of conventional seromucosal cells. The half-moon-shaped cells described in bats (Pinkstaff et al.) present atypical mucous secretion and are interposed between mucosal tubular cells. Four cell types were detected in the gerbil, although the serosal one predominated.

The ductal system of the salivary glands is characterized by three duct classes: intercalary, striated and terminal, with an active participation in the production of saliva. Our results demonstrated the presence of four segments, i.e., intercalary, granulose, striated and excretory ducts, thus differing from the data reported by others. This system also seems to participate in the production and modulation of saliva in an active manner.

The intercalary duct of the gerbil is of small diameter, consists of slightly pavement-like cells, has an intensely stained nucleus and scarce and more eosinophilic and granulose cytoplasm. Similar data were reported by Pinkstaff et al. (1982) for bat glands

The secretory ducts of the submandibular glands of countless mammals have granulose and striated cells arranged in distinct segments (Suddick & Down, 1984); however, our observations revealed the presence of a granulose duct in the submandibular gland consisting of four cell types. Srinivasan & Chang (1974) observed that the size and number of granules in the cells of the granular duct of rats increase with animal age and that the heterogeneity of the granules in the duct cells may indicate the functional diversity of these cells.

The striated ducts are well developed and long in the submandibular gland, consisting of columnar cells with a centralized nucleus and eosinophilic cytoplasm. Their specific characteristic is actually their basal striation (inward indentation of the basement membrane inside the cells among mitochondria elongated in the basal pole) (Tamarin & Sreebny; Pinkstaff et al.; Watanabe et al., 1992).

The present results demonstrated three cell types forming the excretory ducts, which consist of pseudostratified epithelium. Pinkstaff et al. stated that excretory ducts consist of simple columnar epithelium and basal cells which suggest a pseudostratified aspect. They also stated that the all ductal cells present secretory material. Lantini et al. (1990) reported that the excretory ducts of human salivary glands have two cell types. Sato & Miyoshi (1997, 1998 a,b) identified S-shaped or pear-shaped tuft cells with the widened portion close to the nucleus and the narrow one located in the apical and basal portions. These cells reach the basement membrane and contain few organelles, microtubules and tonofilament bundles parallel to the long axis of the cell.

In summary, we may state that the submandibular gland of the gerbil has an ovoid shape, is about 9.0 mm long and 5.9 mm wide and is located in the submandibular region. Histologically, the irregular acini have four cell types and the ductal system consists of four distinct segments: intercalary duct, granulose duct, striated duct, and excretory duct, each with distinct characteristics.

* Department of Morphology - UNOESTE. Brazil.
** Department of Anatomy, ICB-USP. Brazil.
*** Deparment of Morphology, Stomatology and Physiology - FORP-USP. Brazil.

RESUMEN: La morfología de la glándula submandibulardel gerbil fue estudiada macro y microscópicamente. Diez gerbiles fueron anestesiados, perfundidos e inyectados con formalina al 10%. La región cervical anterior de cada animal fue disecada para efectuar el análisis macroscópico de la glándula submandibular. Para el análisis histológico, las piezas fueron fijadas en la misma solución e incluidas en parafina para los procesos de rutina. Cortes seriados de 6-µm fueron teñidos con hematoxilina-eosina y picrosirius, para análisis al microscopio de luz. Los resultados mostraron que la glándula submandibular del gerbil presentaba una forma ovoidea y localizada en la región submandibular, midiendo aproximadamente 9.0 mm de longitud y 5.9 mm de ancho. Histológicamente, cada acino estaba constituido por cuatro tipos de células dispuestas irregularmente. El sistema de ductos constaba de cuatro segmentos distintos: ductos intercalar, granuloso, estriado y excretor.

PALABRAS CLAVE: 1. Glándula submandibular; 2. Morfología; 3.Acinos y ductos; 4. Tejido conectivo; 5. Gerbil- Meriones unguiculatus.

REFERENCES

Bezerra, A. P. C.; Watanabe, I.; Da Silva, M. C. P.; Motoyama, A. A. & Boldrini, S.C. Conventional scanning electron microscopic study of the submandibular gland of the rat. Braz. J. Morphol. Sci., 16:119-23, 1999.         [ Links ]

Espinal, E. G.; Ubios, A. M. & Cabrini, R. L. Freeze-fracture surface of salivary glands of rat observed by scanning eletron microscopy. Acta Anat., 117:15-20, 1983.         [ Links ]

Greene, E.C. Víscera. In: Anatomy of the rat. New York, Hafner, 1959. pp 85-107.         [ Links ]

Lantini, M. S.; Proto, E.; Puxeddu, P.; Riva, A. & Riva, F. T. Fine structure of excretory ducts of human salivary glands. J. Submicrosc. Cytol. Pathol., 22:465-75, 1990.         [ Links ]

Nagato, T.; Nagaki, M.; Kodama, J.; Toh, H. & Tandler, B. The developmental role of type III and type IV cells in the rat submandibular gland. Eur. J. Morphol., 36:123-7, 1998.         [ Links ]

Phillips, C. J. & Tandler, B. Salivary glands, cellular evolution, and adaptive radiation in mammals. Eur. J. Morphol., 34:155-61, 1996.         [ Links ]

Pinkstaff, C. A.;Tandler, B. & Cohan, R. P. Histology and histochemistry of the parotid and the principal and accessory submandibular glands of the little brown bat. J. Morphol., 172:271-85, 1982.         [ Links ]

Sato, A. & Miyoshi, S. Fine structure of tuft cells of the main excretory duct epithelium in the rat submandibular gland. Anat. Rec., 248:325-31, 1997.         [ Links ]

Sato, A. & Miyoshi, S. Cells in the duct system of the rat submandibular gland. Eur. J. Morphol., 36:61-6, 1998a.         [ Links ]

Sato, A. & Moyoshi, S. Topographical distribution of cells in the rat submandibular gland duct system with special reference to dark cells and tuft cells. Anat. Rec. 252:159-64, 1998b.         [ Links ]

Shimono, M.; Satoh, T.; Hashimoto, S.; Inque, T. Freeze-fracture studies of salivary glands. Tokyo Dent. Coll., 33:149-70, 1992.         [ Links ]

Srinivasan, R. & Chang, W. W. The development of the granular convoluted duct in the rat submandibular gland. Anat. Rec., 182:29-40, 1974.         [ Links ]

Suddick, R. P. & Dowd, F.J. Mecanismo de secreção de saliva. In: Menaker, L.; Morhart, R.E.; Navia, J.M. Cáries dentárias-bases biológicas. Rio de Janeiro, Guanabara Koogan, 1984. p.61-97.         [ Links ]

Tamarin, A. & Sreebny, L. M. The rat submaxillary salivary gland: a correlative study by light and electron microscopy. J. Morphol., 117:295-352, 1965.         [ Links ]

Watanabe, I.; Koriyama, Y. & Yamada, E. High-resolution scanning electron microscopic study of the mouse submandibular salivary gland. Acta Anat., 143:59-66, 1992.         [ Links ]

Watanabe, I.; Seguchi, H.; Okada, T.; Kobayashi, T.; Jin, Q. S.; Jiang, X. D. - Fine structure of the acinar and duct cell components in the parotid and submandibular salivary glands of the rat: a TEM, SEM, and HRSEM study. Histol. Histopathol., 11:103-10, 1996.         [ Links ]

Watanabe, I.; Ogawa. K.; Yamada, E. & Konig, J. B. Three-dimensional images of the mouse submandibular gland: na HRSEM study. Anat. Anz., 179:157-60, 1997.         [ Links ]

Dirección para correspondencia:
Prof. Dra. Cristina Mizusaki
Depto de Anatomia
Av. Prof. Lineu Prestes 2415 - Ed. Biomédicas III
Cidade Universitária"Armando Salles de Oliveira"
CEP: 05508-900
Butantã - São Paulo
BRASIL

Tel/Fax: 11 3818 7258

Recibido : 04-01-2001
Aceptado: 05-03-2001

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