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Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.16 n.1 Temuco  1998 

(Cebus apella)

(Cebus apella)

* Tirapelli, L. F.
* Petroni, S.
* Domingues, R. J.
** Tâmega, O. J.

* Post-Graduating - Anatomy - Universidade Estadual Paulista - UNESP - Botucatu - S.P. Brasil
** Professor of Anatomy - IB - Universidade Estadual Paulista - UNESP - Botucatu -SP - Brasil

SUMMARY:In Cebus apella monkeys the salivary submandibular glands are located in the cervical area, side long to the trachea and come morphologically of constituted by four different types of parenchyma cells:

1. Acini: consist of secretory seromucous and mucous cells as well as myoepithelial cell. Secretory cells possesses RER and developed Golgi complex, besides having considerable accumulation of secretion granules what allows a great synthesis capacity to such cells.

2. Intercalated ducts: are characterized by presenting simple cuboidal and myoepithelial cells that connect secretory cells to the grooved ductos, presenting essentially excretory function.

3. Striated ducts: consist of high colunnar cells with extensive folds at its baso-lateral membrane. It presents little amount of RER and of granules what indicates, to this portion, the function of ion and water transport.

4. Ductos excretory: are formed by high colunnar cells made up by the end portion of excretory road.

KEY WORDS: 1. Anatomy; 2. Submandibular gland; 3. Monkey.


Salivary glands in different mammal species have been throughly studied. Such glands were described in carnivores by SHACKLEFORD & WILBORN, 1970; TANDLER & POULSEN, 1976 a,b; COSTA et al., 1981; and mainly in rodents SHACKLEFORD & KLAPPER, 1962; KRONMAN, 1963a, b; DEVI & JACOBY, 1966; FLON & GERSTNER, 1968; FLON, 1973; CHAUDHRY et al. 1985,1986; in hamster ANDREW, 1949; JUNQUEIRA, 1949; TANDLER, 1962; TAMARIN & SREEBNY, 1965; SHACKLEFORD & SCHNEYER, 1971; CHANG, 1974; WATANABE et al.,1992 a,b, 1996; in rats and mices.

On the other hand little is reported regarding salivary glands in non-human primates mainly in monkeys from the new world (platyrrhines) (COWLEY & SHACKLEFORD, 1970; ICHIKAWA & ICHIKAWA, 1977).

Cebus apella described by Linnaeus 1758 is found in a large area of Amazonas State (Rio Negro's basin) as well as in Pará State (Iriri, Counani, Jari and Capim rivers and low part of Tocantins) all in Brazil (COIMBRA-FILHO, 1990). Their eating habit is fruits, sprouts and insects.

The present study has objective to describe morpholically the submandibular gland comparing it to other primates.


Four adult male Cebus apella monkeys were used, weighting about 1.250g from Procriation Nucleus of Monkey - Department of Morphology, School of Dentistry, São Paulo State University, UNESP, Araçatuba, SP, Brazil.

Animals were wighted and previously sedated with ethyl alchool. Right after they were anesthetized with intraperitoneal injection of sodium pentobarbital 30 mg/kg. Fixation was accomplished by perfusion method with glutaraldehyde at 2,5% in blood stream through left ventricle.

Ventral portion of cervical area was cut in order to expose submandibular glands and collect samples.

For light microscopy study the fragments were put in historesina cut 3 micrometes thick and colored by hematoxilina and eosina technique.

In ultrastructural studies samples were damped in araldite M with DDSA (dodecenil-succinico-anidro) and colored by uranila acetate and lead citrate.

Tissue was analyzed and fotographic documented by Olympus Microscope CBB 10 mm/100 at light microscopy and by PHILIPS Microscope EM 301 at electronic microscopy of transmission.


Submandibular gland of Cebus apella has similar location to that of rodents. It is a paired gland, ovid and placed in the ventral portion of cervical area of tubuloacini type which shows seromucous acini and mucous tubules with seromucous demilunes. Inserted ductos are short and scarce segments located between acini and grooved ducts. These last ones join and form larger ducts, the excretory ducts, involved by conjunctive tissue where blood vases are seen.

Ultrastructurally secretory units of submandibular glands are constituted by two different cellular types: seromucous and mucous cells.

Seromucous cells are more numerous and are found forming independent acini or constituting demilunes at the end of mucous tubules. They are pyramidal cells that show cytoplasmatic expansion sideways which extend themselves to variable distances within intercelular tissue space making interdigitations with adjacent cells.

At a more apical part its lateral walls showt inter-celulars canicles defined by microvilli which extend to the lume. A juncional complex blocks the continuity between intercelular tissue space and intercelular canalicles.Luminal surface also shows microvilli while its smooth basal surface is closely juxtaposed to a thin basal sheet.

Basal position nucleus is round and is involved by a great quantity of RER with cisterns organized in a parallel way. Among secretion granules it is observed, at apical area, short segments of RER. Mitochondrias show an enlongated form and are seen dispersed between secretion granules and RER at apical region,at basal area around nucleus and among RER. Golgi complex is seen dispersed at cell perinuclear area between secretion granules and RER.

Secretion granules occupy most of cytoplasm, have an oval form and different dimensions. Its aspect is seen in variable forms and sometimes show electron-dense corpuscles in an eccentric location.

Mucous tubular cells are found in a scarce way among seromucous acini. They show pyramidal form with few lateral specializations among themselves as well as among mucous and seromucous cells at baso-lateral part. On the other hand apical part shows smaller intercelular space and few microvilli. Basal part is in a smooth way.

Nucleus shows a round form and basal position. RER has an extended form and is seen individually all over cytoplasm. Golgi complex is at supero-lateral basal position in relation to nucleus, has an extended form and a parallel placement from its cisterns. Mitochondrias show form and distribution similar to those of its seromucous cells.

Secretion granules occupy a great part of cell showing round form in different sizes and homogeneous distribution and density.

Seromucous demilunes are structures found in the basal portion of mucous tubules separated by a basal sheet what makes them individualiuzed. They are called so due to their shape similar to a semi-moon.

Fig. 1. Photomicrograph of submandibular gland of Cebus apella monkey. General view of glandular parenchyma. Seromucous acini (sa); striated duct (sd); fibroblast (f); conjunctive tissue (ct); mucous tubule (m); blood vase (bv). H.E. 800x.
Electronmicrographs of submandibular gland of Cebus apella monkey.

Fig. 2. General view of glandular parenchyma. Seromucous acini (sa); nucleus (n); mucous tubule (mt); blood capillary (bc). 2750x.

Fig. 3. Seromucous demilunes at mucous acini base. Seromucous acini (sa); mucous tubule (mt). 2750x.

Fig. 4. Myoepithelial cell. Mucous cell (mc); basal sheet (bs); nucleus (n); citoplasmatic projections (cp); conjunctive tissue (ct). 10000x.

Fig. 5. Intercalated duct cells. Nucleus (n). 6500x.

Fig. 6. Striated duct cell. Golgi complex (gc); intercelular space (is); desmossome (d); nucleus (n); mitochondria (m). 13000x.

Fig. 7. Detail of the cell apical portion of striated duct. Desmossome (d); intercelular space (is); secretion granule (sg); lume (l); microvilli (mv); mitochondria (m). 21000x.

Fig. 8. Detail of cell basal portion of striated duct. Baso-lateral interdigi-tation (bi); basal sheet (bs); mitochondria (m). 21000x.

Fig. 9. Detail of mucous cell. Sero-mucous cell (sc); Golgi complex (gc); intercelular space (is); secretion gra-nule (sg); lume (l); nucleus (n); RER (re). 10000x.

Fig. 10. Detail of seromucous cell. Intercelular canicles (ic); Golgi complex (gc); secretion gra-nule (sg); interce-lular junction (ij); nucleus(n). 27500x.

Fig. 11. Detail of apical portion of mucous cell. Interce-lular junction (ij); secretion granule (sg); lume (l); micro-villi (mv). 27500x.

Fig. 12. Detail of basal portion of mucous cell. Secre-tion granule (sg); mitochondria (m); nucleus (n). 8000x.

Fig 13. Detail of apical portion of seromucous cell. Intercelular space (is); secretion granu-le (sg); lume (l); microvilli (mv). 16500x.

Fig 14. Detail of basal portion of seromucous cell. Secretion granule (sg); basal sheet (bs); mitochondria (m); nucleus (n). 13000x.

Intercalated ducts: connect the seromucous acinus and the mucous tubular cells to grooved ducts. They show a cubic form with a well developed nucleus in relation to a reduced cytoplasm. Apical portion turned to lume outstands short microvilli.

They are few amount of organelles and granules in scarce citoplasmatic volume which are seen in the apical portion of these ducts.

Striated ducts: tie the intercalated ones to the excretories. They are made up by a simple colunar epitheliun which shows in its luminal surface short microvilli. Lateral walls, at highest point, have desmossomes what does not occur at baso-lateral portion where it is seen a great quantity of folds contrasting clear and dark interdigitated cellular processes. In dark part a heaped disposition of mitochondrias is evidenced. At basal portion it is noticed the presence of a different basal sheet.

Apical portion is characterized by the accumulation of small vesicles. In the cytoplasm it is observed a spherical nucleus of basal position and around it a well developed Golgi complex. Besides these structures it stands out the presence of great amount of mitochondria all over cytoplasm.

Myoepithelial cells: are extended cells with citoplasmatic prolongations. They are interposed between acinus cells and basal sheet being less frequent in intercalated ducts. Its long lasting citoplasmatic processes involve secretory acini.

Stroma: is formed mainly by conjunctive tissue rich in fibroblastes and collagen fibers with different orientations. The gland is covered by a capsule of conjunctive tissue from which leave septum that divide it in lobes. From these interlobe septum leave conjunctive fibers that involve each acini. In this conjunctive tissue it is observed the presence of a rich capillary net which is involved by an endothelium and underlying it a basal sheet. It is also observed unmyelinated nervous fibers near vase walls.


The location of submandibular gland in Cebus apella monkey is similar to that of rodents, that is to say, in the ventral area of the neck while in the Rhesus monkey and in humans this gland is placed in the angle of jaw close to parotid gland.

Regarding secretory units, as it was observed in Squirrel monkey (Saimiri sciureus) described by COWLEY & SHACKLEFORD (1970), it was noticed in the animal in study, a predominance of seromucous cells in relation to mucous tubular cells when compared to submandibular gland in humans which according to SHACKLEFORD & WILBORN (1968) are formed predominantly by serous acini cells in relation to few mucous cells.

Cebus apella seromucous cells as well as those in Squirrel monkey (Saimiri sciureus) show an extense surface area in apical portion due to presence of prominent microvilli. In contrast, mucous cells are characterized by the presence of few surface specializations.

In the monkey Squirrel (Saimiri sciureus) (KAGAYAMA, 1971) as well as in the animal in study, the citoplasmatic organelles presents differences in its distribution in the seromucous and mucous cells.

RER distribution in seromucous cells is mainly in the basal portion of the cell arranged in a parallel form and on the remaining part of the cell they are found isolated forming small tubules among secretion granules. In rodents RER seen in seromucous cells show a similar distribution to those animals (TAMARIN & SREEBNY, 1965; DEVI & JACOBY, 1966; FLON, 1973; CHANG, 1974; CHAUDHRY et al., 1985).

On the other hand in mucous cells granules have a round form with homogeneous distribution in all over cytoplasm.

In rodents for having only seromucous cells secretion granules are similar to these cell types however not presenting electron-dense corpuscles in its interior (TAMARIN & SREEBNY, 1965; DEVI & JACOBY, 1966; FLON, 1973; CHANG, 1974; CHAUDHRY et al., 1985).

According to COWLEY & SCHACKLEFORD (1970) secretion of seromucous cells in Squirrel monkey (Saimiri sciureus) show low amilase levels when compared to those found in rodents.

Thus, due to feeding habits similar to Squirrel monkey (Saimiri sciureus) the species in study should also present low amount of amilase in the seromucous cells from this gland due to low ingestion of starch in contrast with high production of such enzyme in humans.

It is believed that in Cebus apella monkey the main secretion of seromucous cells is glycoprotein (COWLEY & SHACKLEFORD, 1970).

RESUMEN: En el mono Cebus apella, las glándulas salivales submandibulares se localizan en la área cervical, lateralmente a la tráquea y están constituidas morfológicamente por cuatro tipos de células parenquimatosas que forman diferentes estructuras:

1. Acinos: que presentan células secretoras seromucosas, mucosas y mioepiteliales. Las células secretoras tienen retículo endoplásmico rugoso y complejo de Golgi desarrollados lo que permite a éstas una gran capacidad de síntesis, además presentan una acumulación considerable de gránulos de secreción.

2. Ductos intercalares: se caracterizan por tener células epiteliales cuboidales simples y células mioepiteliales. Los ductos conectan las células secretoras a los ductos granulosos y presentan escencialmente una función excretora.

3. Ductos estriados: consisten en células columnares altas con pliegues extensos en su membrana en las zonas basal y lateral. Presentan una cantidad pequeña de retículo endoplásmico rugoso y de gránulos, lo que sugiere una función de transporte de iones y agua.

4. Ductos excretores: constituidos por células columnares altas y forman la porción final de la vía excretora.

PALABRAS CLAVE: 1. Anatomía; 2. Glándula submandibular; 3. Mono.


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Dirección para correspondencia:
Prof. Dr. Luis Fernando Tirapelli
Universidade Estadual Paulista
Campus Botucatu
Instituto de Biociências
Departamento de Anatomía
CEP 18618-000
Botucatu - SP

Recibido : 26-03-1998
Aceptado: 22-04-1998

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