SciELO - Scientific Electronic Library Online

Home Pagelista alfabética de revistas  

Servicios Personalizados




Links relacionados


Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.20 n.1 Temuco  2002 

GLAND DUCTS (Cebus apella, LINNAEUS 1766)


Alexandre Roriz Blumenschein & Jussara Rocha Ferreira

Universidade Federal de Goiás, Brasil
Financial Support: Fundação de Apoio a Pesquisa - FUNAPE / UFG

SUMMARY: In this study, anatomic aspects of thirty (30) submandibular salivar glands excretory ducts from the monkey Cebus apella were studied by dissection techniques with magnifying glass. The monkey heads (obtained from previous researches) were all injected with green stained latex solution (neoprene 450). This procedure consists in: the animal's anesthesia; withdrawal of blood; cannulation of the aorta in cranial and caudal sense; perfusion with warm water (40°C); injection of the arterial system with stained latex; conservation in formaldehyde solution (10%) and immersion in nitric acid (2%) for a period of 10 days with the intention of decalcifying the jaw bone so that dissection was made easier. The submandibular main duct is formed by the confluence of small ducts that emerge from the glandular acinus. The main duct leaves the gland by its hilum, accompanied by vascular-nervous structures. It proceeds in rostral direction towards the sublingua, it's proximal part located above the digastric muscle's tendon and it's distal two thirds covered by the milo-hyoid muscle. The duct maintains close relation with the sublingual gland's parenchyma, and is positioned infer-medially to this gland. The duct proceeds in each antimer to the base of the sublingua, and from this point on, is directed antero-medially anastomosing with the contralateral duct (26,67%) or ending freely (73,33%) on the sublingual mucosa through a small orifice. A morphologic pattern of these submandibular ducts in Cebus apella can be traced upon the data analyzed, permitting a comparison with other species since no significant differences between the antimers were found.

KEY WORDS: 1. Submandibular salivar glands; 2. Submandibular ducts; 3. Cebus apella.


Brazil is the largest natural habitat for primates in the world; thus, scientific studies about species that occupy the different ecologic niches in the country are essential for the protection of these species in  wildlife. The submandibular glands have been referred to in the literature by various authors. Hill (1953, 1955, 1957, 1962 and 1966) observed the Old World Monkeys. In strepsirhines, the author refers to a pair of mucous folds, the frenal lamella, localized below the sublingua that superposes the salivar gland ducts. In haplorhini there isn't a sublingua, and this structure is vestigial in tarsius. These animals own a short, sometimes bifid papilla that represents the anterior portion of the frenal lamella where the submandibular gland ducts end. In Pithecoidea there is a frenal lamella that represents mucous folds in which discharge submandibular ducts, instead of a sublingua. The dorsum of this lamella may present a crest, noticed for example in the tongue's median ventral sulcus of Cebus. In Aotes the submandibular gland is simple, with a long duct, much like the glands in lemures. In Alouatta the submandibular gland is rounded and compact, localized in the space between the jaw's angle and cervical portion of the parotid gland. The submandibular duct in this case proceeds in the usual manner, discharging below the lingual frenum. In Brachyteles the submandibular gland has superficial and deep portions, being the superficial one the bigger portion that forms a smooth, ovoid mass near the jaw's angle. This portion may be subdivided by the submandibular duct into medial (bigger) and lateral (smaller) portions, as seen in Ateles. In Cercopithecus the submandibular gland is a compact and ovoid mass with some accessory lobules localized below the angular region of the jaw, being its rostral extremity localized deeply below the jaw. In C. cephus, bilateral asymmetry regarding the size of the gland is present; its duct emerges from the hilum localized in the anterior part of the gland's deep surface. This duct then follows its usual course, discharging in the buccal cavity next to the lingual frenum (parafrenular papilla).

In Miopithecus, Riviniam's ducts discharge directly in the buccal cavity, situated superficially to Bartoliniam's gland, whose duct runs side by side with Wharton's duct, as seen in Cercopithecus. In Cercocebus (Hill, 1970) the submandibular gland, localized between medial pterygoid, digastric and stilo-hyoid muscles, is compact, non divided, elongated, with an oval body, having it's posterior margin projected beyond the jaw's angular region in apposition to the aerial laryngic sack. A relatively large duct emerges from this gland's hilum,  being curved upward and then proceeding onward medially to the sublingual gland. Some isolated glandular lobules are found neighboring the arched portion of the duct, thus nothing comparable with structures found in Papio or Macaca nemestrina. The duct discharges at the tip of the corespondent frenal lamella, next to the lingual papilla.

In Macaca  the submandibular gland in M. irus is globe-shaped, resembling a large bean, and kept in a capsule of deep cervical fascia. A separate duct follows the dorsal edge of the principal parotid duct, joining it halfway between the intersection of the lingual nerve and the plica sublingualis. The common large duct is unified near its end to the major sublingual duct, discharging in the plica by a single orifice, common to the three glands. The submandibular gland is distinct in Tupaia (Hill, 1972 a and b). In Ptilocercus the sublingual gland isn't present as a distinct structure, but represented by anterior lobules of the submandibular gland (Le Gross Clark, 1962). The submandibular gland is the main gland in Lemur, Microcebus, Indri, Daubentonia, Galago and Tarsius (Fahrenholz, 1937).

In Theropitecus (HILL, 1972 a and b) there is a firm, cone shaped, incipiently bifid projection (frenal lamella), whose lateral edgings are separated from another elongated lateral elevation by a deep sulcus. A plica sublingualis surpasses this structure, and a lobular papilla flattened dorso-ventrally is noted on both sides. This is where the submandibular gland duct discharges. The duct is large and has a course medial to the sublingual gland, discharging in a rugose papilla, infero-laterally to the frenal lamella.

The literature doesn't inform well about the origin, course and way of dischargement of Cebus apella´s submandibular gland ducts. Thus, by describing these structures we intend to contribute with data of it's morphology which will be useful in the semiologic exams of this specie's neck region. By describing the submandibular gland ducts in Cebus apella, we intend to collaborate to the scientific field with data of its morphology, and in the ethical field by preserving nature.


The method is based on techniques of macroscopic observation with magnifying glass. Thirty glandular antimers were observed in fifteen monkey heads already separated from the rest of the animal's body. These monkey heads, used in earlier studies, were provided by the Faculty of Veterinary Medicine and Zootechny from the University of São Paulo (F.M.V.Z / USP). This material was collected in a period of 10 years time in São Paulo's zoo, from animals that died naturally or by accident. The Faculty usually keeps parts of animals utilized in other studies, so that new studies can be made upon this material. This being, we contributed in the ethical field by preserving nature, not needing to sacrifice any animals for this study, since we used animal parts already used in other studies, themselves being collected only in case of natural death or death by accident of these monkeys. All the monkey heads went through injection of the toracic aorta, so that blood vessels could be studied properly. The routine technique utilized was: the animal's anesthesia; withdrawal of blood; cannulation of the aorta in cranial and caudal sense; perfusion with warm water (40°C) and injection of the arterial system with stained latex. Fixation and conservation of the heads was made in aqueous formaldehyde solution (10%). The heads were immersed in nitric acid (2%), for a period of ten days, causing jaw decalcification, so that dissection with esteoscopic microscope (40x) was made easier.

The data referring to the origin, course and dischargement of the submandibular ducts were registered through schematic models made from each head dissected. An adequate nomenclature for the ducts we described in neotropic primates was not found in the literature, thus we opted by naming them according to their function in the material we described. The following terms were utilized: submandibular duct; salivar submandibular gland; intra-parenchymary submandibular ducts; contralateral submandibular duct; sublingual gland; sublingua and tip of sublingua. These terms are a suggestion for the nomenclature of these structures in Cebus apella, since there isn't yet a defined Primatological Nomina. 


The origin, course and place of dischargement of the submandibular gland ducts of Cebus apella were studied in this paper. In this animal the gland has a round-shaped, volumous and lobular structure, circumscribed by connective tissue in the digastric triangle, its superficial portion situated below the jaw and its deep portion situated laterally to the milo-hyoid muscle. The superficial portion is covered by the following order of structures: the deep fascia, platism muscle, subcutaneous tissue and skin. Some submandibular lymph nodes are localized superficially to the gland. The facial vein crosses the gland postero-inferiorlly and the facial artery compresses the gland on its posterior surface, giving out a branch that feeds the gland: the submandibular artery.

The gland's deep portion extends itself above the superior surface of the milo-hyoid muscle, at the same level of the sublingual gland. Medially, the gland bears relation to the hypoglossal and lingual nerves. The confluence of small tubes originated in various glandular lobules, form, by anastomosing themselves in a branch-like pattern, the main submandibular duct. This duct is unique, and steers superficially, emer-ging and going onwards in rostral sense. These tubes that are confluent in the direction of the glandular hilum, forming the submandibular main duct, are accompanied in their intra-parenchymal course by blood vessels responsible for the gland's blood supply. When it finally emerges from the glandular hilum, the subman-dibular main duct steers in a rostral sense, from the base to the tongue's apex, ending in the tip of the sublingua (bifid in this animal), where it dischar-ges its salivar secretion. In the thirty submandibular glands we observed, the main glandular duct was formed by the confluence of smaller, intra-paren-chymal tubes in 100% of the cases.

The duct emerges from the gland in the same place that the submandibular artery penetrates the gland (Fig. 2). The duct in it's caudal portion is located above the digastric muscle's tendon, and follows in rostral sense medially to the sublingual gland, or sometimes goes through the sublingual gland's parenchyma, mixing with it, on the way to the sublingua (Fig. 1). In its anterior portion the milo-hyoid muscle covers the duct. From the thirty glands analyzed, we observed two different patterns concerning the duct's course:

Fig. 1. Photography of the supra-hyoidean region of Cebus apella, ventral view, observation 9, where can be identified: 1. The tongue; 2. Sublingua; 3. Sublingual gland; 4. Jawbone; 5. Submandibular gland duct emerging from the parenchyma; 6. Following in rostral sense; 7. Towards it's place of dischargement in the sublingua.

Fig. 2. Photography of the supra-hyoidean region of Cebus apella, ventral view, observation 10, where can be seen: 1. The relation of the submandibular gland duct; 2.with the submandibular artery; 3. in the glandular hilum region; 4. The submandibular gland; 5. Sublingua; 6. The duct´s course, isolated from the submandibular artery, steering towards the sublingua´s apex.

a)  The submandibular duct emerging from the gland's hilum, steering rostrally, and discharging freely by the tip of the bifid sublingua in 73,33% of the cases in both antimers (Obs.: 1, 3, 4, 5, 6, 8, 10, 11, 12, 13 and 15);

b) The submandibular duct from one antimer anastomosing itself with the contralateral duct from the other antimer, just before they arrive in the sublingua, observed in 26,67% of the cases (Obs.: 2, 7, 9 and 14).

Independently if the ducts anastomose themselves or not with the opposite antimer, they always (100%) end discharging on the tip of the sublingua. In its rostral course, the ducts are localized supero-medially to the lingual nerve.

The left and right ducts, as they get closer to the sublingua, curve themselves antero-medially in the underlying connective tissue, detouring from the topographic relation they had with the sublingual salivary glands. The dischargement orifice of the duct in the tip of the sublingua is frequently identified macroscopically in the fixed piece. Another aspect analyzed was that the gland presented considerable hypertrophy in adult individuals, in relation to the animal's age and dental arch. This observation is not entailed to any data in relation to the animal's alimentary habits mainly because we didn't have access to these habits. We judged registering this fact important, even though it isn't a proposal for this analysis, since this fact doesn't interfere in the behavior of the morphology presented by the ducts that were studied.

Fig. 3. Schematic representations of Cebus apella's submandibular gland ducts dissections: 1. The subman-dibular glands; 2. Submandibular gland ducts; 3. Sublingual glands; (®) The anastomose between the antimers; 4. Dischargement of the duct; 5. On the tip of the sublingua.


We will discuss our results by comparison with other papers about origin, course and dischargement of the submandibular gland ducts of Cebus apella. The papers studied permit an analysis about the terminology, origin, course and dischargement of these ducts that leave the submandibular gland and head towards the sublingua.

Considerations about terminology.

We verified that the tendency while analyzing and interpreting data about salivary glands in primates is to describe other animals having the human model as the standard model. This is not always adequate since the adaptations in each group respect the harmonious relationship of the ecosystem according to the ontogeny and phylogeny of each group, and therefore leading to different paths among these groups. This monkey (Cebus apella) is an omnivorous creature, having varied alimentary habits. In times of scarceness of food, this animal eats seeds and fibers. The evident macroscopic hypertrophy of the salivar glands demonstrate this fact. The caliber of these ducts indicates the passage of a lot of salivary fluid during the masticatory process, thus lubricating well the food. The presence of a sublingua represents a structure that facilitates the spread and dispersing of saliva in the mouth cavity. The morphology observed showed that the duct runs by the sublingua´s border, below the tongue and laterally to the tongue's base muscular group. These lingual muscles and their movements would force the saliva to flow faster inside the duct. The terms: submandibular duct, sublingual duct and intra-parenchymal ducts seem like adequate reference to these structures. We refered to the topographic relationship of the submandibular ducts with the sublingual gland, since the sublingual gland's small ducts incorporate themselves to the main submandibular duct, discharging in the sublingual apex, according to the literature: Hill (1953, 1955, 1957, 1962, 1966) in primates and Sicher & DuBrul (1977) in human primates.

We observed in this animal the formation of a duct that emerges through the glandular hilum in the inferior surface of the medial gland border, seemingly to what Hill (1970) described in Cercocebus. It seemed to us evident that although the authors had analyzed ducts and glands of various primates, there wasn't uniformity in the denomination of these structures, making us consider using the terms: submandibular salivary gland and accessory submandibular salivary gland. We considered that the glands are relatively symmetrical between the opposing antimers and are round shaped, refuting the findings of Hill (1957, 1966) in C. cephus were the author refers to bilateral asymmetry of glandular size, while in Macaca irus describes it resembling a large "bean" and Le Gros Clark finding in Ptilocercus a lobular structure. We opted by naming the duct of dischargement: submandibular duct and accessory submandibular duct for Cebus apella. This duct was named Wharton's duct in Cebus by Hill (1953, 1957), and in Macaca nemestrina and Papio is refered to as the arched portion of ducts that emerge of isolated lobules of glandular tissue. The denomination of the submandibular salivar gland and its ducts wasn't considered by the authors, although in human primates this gland and its ducts are described and nominated as submandibular gland and submandibular gland duct (Warwick & Williams, 1979); superficial and deep lobes of the submandibular gland and submandibular duct (Johnson & Moore, 1997); submandibular gland, submandibular tube and sublingual caruncle  (Sicher & DuBrul); and submandibular gland and submandibular duct (Madeira, 2000). The option of adopting the term accessory submandibular duct in Cebus apella is based on the fact that Oliveira et al. (2000) found accessory glands with independent arteries in this species.

Considerations about submandibular duct's origin, course and way of dischargement.

The study of origin and course of the submandibular ducts wasn't deepened by the authors, who made only general descriptions about the subject. Hill (1966, 1970) observes that in Cercopithecus and Cercocebus the submandibular duct emerges from the glandular hilum in the anterior part of the deep surface of the gland. We verified that in 100% of the cases, the duct emerges from the glandular hilum, accompanied by vascular and nervous structures that normally arrive or leave the gland. The submandibular artery's subdivisions accompany the confluence of intra-parenchymary submandibular ducts, in their glandular hilum sense. When both the main duct and the artery find themselves out of the glandular parenchyma; the duct follows in rostral sense towards the sublingua accordingly to our observations and the artery emerges from the facial artery accordingly to the observations of Oliveira et al., to afterwards penetrate the glandular parenchyma.

Hill (1962, 1970 and 1972b) in cebidean monkeys, while analyzing the course of the duct, describes only that after leaving the hilum the duct curves upwards primary, running medially to the sublingual gland on it's way to the place of dischargement. In human primates Sicher & DuBrul recognize a submandibular channel that emerges from the internal superior part of the gland and steers onwards accompanied by an anterior extension of the gland that crosses the lingual nerve superiorly, while Johnson & Moore refer to a submandibular duct, that initiates in the superficial lobe, running onwards in intimate relation with the lingual nerve, firstly between the milo-hyoid and hiogloss muscles, and secondly between the gland and geniogloss muscle.

Differing from these authors, we recognized in Cebus apella a submandibular duct that leaves the gland in its infer-medial portion, being the glandular parenchyma entirely contained by the glandular capsule, in a way that the duct after it's departure from the gland steers freely with other elements of the glandular pedicle. The duct shares intimate topographic relation with the sublingual glandular parenchyma, nearby to the jaw's division, although we couldn't observe, as Sicher & DuBrul did, that this duct joins the more calibrous channel that comes from the sublingual gland. On the contrary, Johnson & Moore relate that sublingual glandular channels open in the sublingua through many (15) small ducts. We noted that the duct's course in Cebus apella, runs medially or sometimes mixing itself with the sublingual glandular parenchyma. On the other hand, we didn't observe if the submandibular duct receives any confluence, or even relates with sublingual glandular ducts, as was noticed in other primates by the authors (Hill, 1966 and Warwick & Williams). We observed anastomoses (26,67%) between the two ducts of significant caliber. The remaining 73,33% of cases represent ducts that follow directly to the sublingual apex, without anastomosing themselves. Other authors noted nothing similar.

Various papers relate to the way of dischargement of submandibular ducts. Hill (1953, 1955, 1957, 1970, 1972 a and b) observes that in the different primates, the submandibular ducts usually discharge in a papilla situated anteriorly to the frenal lamella, discharge in the own lamella, or in the plica sublingualis. The author comments that numerous times this papilla is wrongly mistaken with the sublingua. In stresirhines the duct discharges in the frenal lamella below the sublingua; next to the lingual frenum in C. cephus; and in Miopithecus directly in the buccal cavity. In the meantime, Sicher & DuBrul in humans, refer to the dischargement of the duct in the sublingual caruncle, named sublingual papilla by Johnson & Moore in their work.

We observed that in 100% of the cases, the submandibular ducts discharge in the apex of a truly bifid sublingua, being that each duct discharges at one of the tips of the bifid sublingua. We noted that the orifice from where the salivary content is dispersed in the buccal cavity is often seen macroscopically. The interpretation of the data in Cebus apella indicates a significant stability in the findings. We worked with a larger number of individuals than the various authors consulted; believing that the morphology concerning the way of formation, origin, course and dischargement of the salivary submandibular gland ducts in both antimers was certainly characterized.

We believe we can conclude the following facts: the submandibular salivary gland ducts in Cebus apella originate from a confluence of smaller ducts that emerge from the glandular acinus and anastomose towards the glandular hilum, forming a single main duct: the submandibular duct. The ducts in both antimers depart from the gland and steer to the tongue's base, having relationship medially with the tongue's base muscular group, and laterally with the sublingual gland, being positioned superiorly to the digastric muscle's tendon in its caudal portion and being covered by the milo-hyoid muscle in its anterior portion. While emerging from the glandular acinus, the intra-parenchymal ducts are accompanied by branches of the submandibular artery. While leaving the glandular hilum localized in the infer-medial surface of the gland, the submandibular duct perforates the connective capsule in a short descending trajectory, curving anteriorly in rostral sense. In the medium portion of the duct trajectory, between the gland and the sublingua, the lingual nerve and adjacent blood vessels accompany the duct.

RESUMEN: Algunos aspectos anatómicos de los canales excretores de 30 glándulas submandibulares de "macaco prego", Cebus apella, estudiamos por técnicas de disección en lupa. Las cabezas fueron inyectadas con solución de látex (neoprene 450) y coloradeadas con pigmento verde. Con el propósito facilitar la disección, descalcificamos las mandíbulas, utilizando el siguiente procedimiento: anestesia del animal; retirada de la sangre: canulación de la aorta en sentido craneal y caudal; perfusión con agua tibia (40ºC); inyección del sistema arterial con látex; fijación en formol al 10% e inmersión en ácido nítrico al 2% por 10 días. Observamos que el conducto submandibular estaba formado por la confluencia de pequeños conductos que emergían de los acinos glandulares. El conducto dejaba la glándula por su hilio, acompañado de las estructuras neurovasculares. Seguía hacia rostral, hasta la parte inferior de la lengua, estando su parte proximal localizada arriba del tendón del músculo digástrico y los dos tercios distales, recubiertos por el músculo milohioídeo, manteniendo íntima relación con el parénquima de la glándula sublingual y ubicándose ínfero-medialmente a ésta. Los conductos de cada glándula se unían en el 26,67% de los casos o desembocaban libremente en el 73,33% de ellos, en la mucosa bajo la lengua, a través de un pequeño foramen. Los datos analizados trazan un patrón morfológico de estos conductos submandibulares en el Cebus apella. No existen diferencias significativas entre los antímeros, permitiendo la comparación con otras especies.

PALABRAS CLAVE: 1. Glándulas salivales submandibulares; 2. Conductos submaxilares; 3. Cebus apella.


Fahrenholz, 1937 apud HILL, 1972, p.  93.

Hill, W.C.O.  Primates, Comparative  Anatomy  and Taxonomy. I:  Strepsirhini. University  Press, Edimburgh,  1953. pp. 73-4 and 289-90.                   [ Links ]

Hill, W.C.O.  Primates,  Comparative  Anatomy   and  Taxonomy.  II:  Tarsioidea,  Haplorhini. University Press, Edimburgh, 1955. pp. 51-4.         [ Links ]

Hill, W.C.O.  Primates,  Comparative   Anatomy  and  Taxonomy.  III:  Platyrrhini, Pithecoidea.  University  Press, Edimburgh, 1957.   pp. 40-4.         [ Links ]

Hill, W.C.O. Primates, Comparative  Anatomy  and  Taxonomy. V, part. B: Cebidae. University  Press, Edimburgh, 1962. pp. 320-2.         [ Links ]

Hill, W.C.O. Primates, Comparative Anatomy and Taxonomy. VI: Cercopithecinae, Catarrhini.  University Press, Edimburgh, 1966. pp. 318-20.         [ Links ]

Hill, W.C.O. Primates, Comparative  Anatomy   and  Taxonomy. VII: Cercocebus, Macaca,  Cynopithecus. Cynopithecinea. University Press, Edimburgh, 1970. pp. 86-108.         [ Links ]

Hill, W.C.O.  Primates, Comparative Anatomy and Taxonomy. VIII: Papio, Mandrillus, Theropithecus.  Cynopithecinea. University Press, Edimburgh, 1972 a. pp. 130-2.         [ Links ]

Hill, W.C.O.  Evolutionary Biology of the Primates. Academic Press, London, 1972b. pp. 91-3.          [ Links ]

Johnson, D. R. &  Moore, W. J. Cavidade da boca e estruturas relacionadas. In: Anatomia para  Estudantes de Odontologia. 3. ed. Guanabara Koogan: Rio de Janeiro, 1997. pp. 181-9.         [ Links ]

Le  Gros  Clark,  W.N.  The Antecedents  of  Man. 2. ed. University Press, Edimburgh, 1962. p. 172.         [ Links ]

Madeira, M.C.  Boca. In: Anatomia da face / bases anátomo-funcionais para a pratica odontológica.  3. ed. Sarvier, São Paulo. 2000. pp. 129-36.         [ Links ]

Oliveira,  A. S.; Blumenschein, A.R. & Ferreira, J. R.  Estudo anatômico do modelo arterial de  vasos responsáveis pelo aporte sanguíneo da glândula submandibular de primatas neotropicais [Cebus apella, Linnaeus, 1766]. Acta Scientiarum  22(2):573-9, 2000.         [ Links ]

Sicher, H. & DuBrul, E. L.  Glândulas da cavidade bucal. In: Anatomia Bucal. 6. ed. Guanabara Koogan, Rio de Janeiro, 1977. pp. 200-4.         [ Links ]

Warwick, R. &  Williams, P. L.  Gray Anatomia. 35. ed. Guanabara Koogan, Rio de Janeiro, 1979.         [ Links ]

Correspondence To:
Prof. Dra. Jussara Rocha Ferreira
Rua 111 Nº 250 Sector Sul
Goiânia - GO

Recibido : 02-08-2001
Aceptado: 25-02-2002

Creative Commons License Todo el contenido de esta revista, excepto dónde está identificado, está bajo una Licencia Creative Commons