The Veterinary Journal the Veterinary Journal 175 (2008) 379–383

Available online at www.sciencedirect.com The Veterinary Journal The Veterinary Journal 175 (2008) 379–383 www.elsevier.com/locate/tvjl

The buccal lymph node (lymphonodus buccalis) in dogs: Occurrence, anatomical location, histological characteristics and clinical implications

Christophe R. Casteleyn a,*, Maartje van der Steen a, Jan Declercq b, Paul Simoens a

a Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium b Department of Small Animal Medicine and Clinical Biology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium

Accepted 28 January 2007

Abstract

Three dogs were presented for clinical examination with bilateral buccal nodules which were identiﬁed as enlarged buccal lymph nodes. As little is known about this pathology, 150 dogs were examined by anatomical dissection for the presence of buccal lymph nodes. They were found in 13 dogs, occurring bilaterally in six dogs and unilaterally in seven dogs. Two buccal lymph nodes were bilobulated and one was double. The lymph nodes were always located dorsal to the zygomatic muscle and rostral to the masseter muscle in the region where the superior labial vein drains into the facial vein. Histology demonstrated a large amount of intranodal adipose tissue scattered throughout the lymphoid tissue. The canine buccal lymph node should not be confused with the accessory parotid or ventral buccal salivary gland and is clinically important as it can enlarge due to tumour metastasis or inﬂammation of the buccal region. Ó 2007 Elsevier Ltd. All rights reserved.

Keywords: Anatomy; Buccal nodule; Dog; Histology; Lymphatic system

1. Introduction skin biopsy specimens revealed cutaneous non-epitheliotropic lymphoma. A 7-month-old Afghan hound, a 3.5-month-old New- The anatomical features and possible pathology of buc- foundland pup and an 8-year-old Shar pei were presented cal lymph nodes are poorly documented. Rumph et al. for evaluation of bilateral nodular lesions in the buccal (1980) described a clinical case of a 4-month-old male Lab- region (Figs. 1a, 1b and 1c). The nodules, which were not rador Retriever presented with masses rostroventral to painful in any of the dogs, ranged from 1 to 2 cm in diam- each eye. The masses were periodically swollen, but seemed eter and were diagnosed as enlarged buccal lymph nodes. not to induce any disease. Based on this clinical case, the In the Afghan Hound, clinical examination revealed no authors systematically looked for similar masses and found other abnormalities and the buccal lymph nodes spontane- them in 15/171 examined Greyhounds. After histology, ously regressed. The Newfoundland pup had a subcutane- they concluded that the masses were lymph nodes which ous abscess in the right upper lip. The Shar pei suﬀered they named the facial lymph node. Shelton and Forsythe from generalized peripheral lymphadenopathy and subse- (1979) performed a similar study and found the lymph quently showed nodular lesions in the ears, the anal region node, which they called the buccal lymph node (lymphono- and the perivulvar fold. Histopathological examination of dus buccalis), in 22/250 dogs of various breeds, ages and sex. Both the studies of Shelton and Forsythe (1979) and * Corresponding author. Tel.: +32 9 264 77 15; fax: +32 9 264 77 90. Rumph et al. (1980) have been brieﬂy reviewed by Evans E-mail address: [email protected] (C.R. Casteleyn). (1993). Adams (1986) illustrated in a textbook drawing

in the literature and because of its possible clinical implications, a screening was performed to determine its prevalence, exact anatomical location and histological characteristics.

2. Materials and methods

The buccal regions of 150 dogs of various breeds, age and sex, euthanased for reasons other than this study, were examined macro- scopically (Table 1). Photographs of each presumed buccal lymph node were taken using a digital camera (Canon EOS 300D) and samples for histological analysis were fixed in 3.5% buffered formaldehyde for 1 week followed by paraffin wax embedding using a histokinette (Shandon Citadel 1000, Thermo Electron). Tissue sections (8 lm thick) were made, mounted on slides, stained with haematoxylin (Hematoxylin C.I. 75290, Merck) and Fig. 1a. Bilateral enlargement of buccal lymph nodes (arrows) in an eosin (Eosine yellow C.I. 45380, VWR International) and examined with a Afghan hound due to unknown aetiology. motorized microscope (Olympus BX 61) linked to a digital camera (Olympus DP 50).

Table 1 Occurrence of the buccal lymph node in 150 dogs of various breeds Breed Number Unilateral Bilateral of dogs presence of presence of examined buccal buccal lymph node lymph node American Staffordshire Terrier 10 0 0 Basset Hound 1 0 0 Beagle 2 0 0 Belgian Malinois 5 0 0 Belgian Tervuren 1 0 0 Berner Sennen 4 1 0 Boerboel 1 0 0 Fig. 1b. A 4-month-old Newfoundland pup with enlarged buccal lymph Border Collie 1 0 0 nodes caused by abscessation of the right upper lip (arrow). Bouvier des Flandres 3 1 0 Boxer 2 0 0 Bull Terrier 1 0 0 Collie 1 0 0 Dalmatian 1 0 0 Doberman Pincher 4 1 1 Dogue de Bordeaux 2 0 0 English Bulldog 1 0 0 Flat Coated Retriever 1 0 0 German Pointer 1 0 0 German Shepherd Dog 12 2 1 Giant Schnauzer 1 0 0 Golden Retriever 6 0 3 Great Dane 2 0 0 Groenendaler 1 0 0 Irish Setter 1 0 0 Jack Russell Terrier 9 0 0 Keeshond 1 0 0 Labrador Retriever 12 2 0 Fig. 1c. Bilaterally enlarged buccal lymph nodes (arrows) in a Shar pei Maltese 1 0 0 suffering from a cutaneous non-epitheliotropic lymphoma. Mongrel 41 0 0 Napolitan Mastiff 2 0 0 an anonymous but apparently similar lymph node located Newfoundland 3 0 0 Pekingese 1 0 0 rostral to the angle of confluence of the facial and the supe- Rottweiler 9 0 0 rior labial veins. Saint Bernard 1 0 0 The buccal lymph node has been described in various Shar pei 2 0 1 other species including humans, primates, rabbits, guinea Siberian Husky 1 0 0 pigs, rats and camels (Barone et al., 1950; Spira, 1962; Standard Poodle 1 0 0 Weimaraner 1 0 0 Grasse´, 1972; Grau, 1974; Barone, 1996). Since the presence of the canine buccal lymph node is rarely documented Total 150 7 6 C.R. Casteleyn et al. / The Veterinary Journal 175 (2008) 379–383 381

For reference, samples were also taken from the mandibular and parotid lymph nodes and from the parotid, accessory parotid and ventral buccal salivary glands.

3. Results

3.1. Prevalence and macroscopic characteristics

In 2/150 examined dogs, the buccal lymph nodes were enlarged causing a swelling which could be palpated through the skin. After dissection, the buccal lymph nodes were found in 13 dogs (i.e. 9% of all examined dogs). The lymph nodes were bilaterally present in six dogs and unilaterally in seven dogs, more specifically four times on the left Fig. 3. Bilobulated buccal lymph node (arrows) located medial to the side and three times on the right side of the head (Table 1). superior labial vein. Notice the position of the buccal lymph node at the Two out of the total number of 19 observed buccal lymph level of the fourth premolar (P4) in the right upper jaw of a German nodes were bilobulated and one was double. Shepherd Dog. The lymph nodes were always located dorsal to the zygomatic muscle and rostral to the masseter muscle in the region where the superior labial vein drains into the facial vein (Fig. 2). The buccal lymph node was located rostral to the facial vein in seven cases: once dorsal to the superior labial vein in the angle of confluence of the facial and superior labial veins, once medial to the superior labial vein (Fig. 3), four times directly ventral to the angle of confluence of the facial and superior labial veins (Fig. 4a), and once more caudal to the angle of confluence. In one case the lymph node was located medial to the facial vein where the superior labial vein joined the facial vein. In the other 11 cases, the lymph node was located caudodorsal to the facial vein: four times directly caudal to the angle of confluence of the facial and superior labial veins, and seven times ventral and distinctly caudal to the angle of confluence Fig. 4a. Drawing of the canine head showing a buccal lymph node located (Fig. 2). The distance between the angle of confluence directly ventral to the angle of confluence of the facial and superior labial and the buccal lymph node varied from 2 to 10 mm. The veins. Some landmarks of the buccal area are additionally represented: ln. variable position of the observed canine buccal lymph buccalis (1), lnn. mandibulares (2), ln. parotideus (3), gl. parotis (4), gl. nodes is illustrated in Fig. 4b. parotis accessoria (5), gl. mandibularis (6), m. zygomaticus (7), m. masseter The size of the buccal lymph nodes was variable with the (8), m. buccinator (9), m. orbicularis oris (10), v. jugularis externa (11), v. maxillaris (12), v. facialis (13), v. labialis inferior (14), v. labialis superior long rostrocaudal axis ranging from 5 to 24 mm, the short (15), v. lateralis nasi (16). dorsoventral axis from 3 to 14 mm, and the thickness from 1 to 5 mm.

Fig. 2. Localisation of the buccal lymph node (arrow) in a Doberman Fig. 4b. Compilation drawing of the canine head showing the variability Pincher in relation to the facial (1) and superior labial (2) veins and the of the buccal lymph nodes which are located nearby (black dots) or medial zygomatic (3) and masseter (4) muscles. to (white dots) the facial or superior labial vein. 382 C.R. Casteleyn et al. / The Veterinary Journal 175 (2008) 379–383

3.2. Histological characteristics trast, the mandibular and buccal salivary glands consisted of sero-mucous acini. In one case, a presumed canine buc- The typical lymph node architecture was not always eas- cal lymph node was identified as a ventral buccal salivary ily recognisable in histological sections of the canine buccal gland by means of histology. lymph nodes (Figs. 5a and 5b). However, all lymph nodes Reference samples taken from mandibular and parotid were encapsulated by connective tissue composed of colla- lymph nodes revealed the typical architecture of a lymph gen and fibroblasts with trabeculae radiating into the node. node, consisting of a capsule and trabeculae, the cortex Smooth muscle cells, capillaries and adipose tissue could containing subcapsular sinuses and primary and secondary frequently be observed in the trabeculae. In 11 buccal lymph follicles, and the medulla containing medullary lymph nodes, a cortical and medullary layer could be dis- cords and sinuses. tinguished. The cortex was largely filled by diffuse lymphatic tissue and with primary and secondary lymph follicles. 4. Discussion Subcapsular sinuses were detected at the periphery of the cortex, just underneath the capsule. The medulla was com- With regard to nomenclature, the lymph node in the posed of medullary cords and sinuses. In all canine buccal buccal region has for many years been called ln. facialis lymph nodes, varying amounts of adipose cells were dis- in guinea pigs (Spira, 1962) and dogs (Rumph et al., tributed throughout the lymphoid tissue. In contrast, the 1980). On the other hand, authors such as Shelton and reference samples from the mandibular and parotid lymph Forsythe (1979) use the term ln. buccalis. This nomencla- nodes contained only few adipose cells which were mainly ture confusion has recently been resolved by the Interna- located in the trabeculae. tional Committee on Veterinary Gross Anatomical Nomenclature by officially recognizing the term ‘‘ln. buccalis’’ belonging to the Lymphocentrum mandibulare (Nom- 3.3. Reference samples ina Anatomica Veterinaria, 2005). The present study revealed that the buccal lymph node is Both the parotid gland and the accessory parotid gland, only present in a minority of dogs. The observed preva- which was usually present in close association to the paro- lence of 9% is in accordance with the findings of Shelton tid duct, were composed of serous glandular tissue. In con- and Forsythe (1979) and Rumph et al. (1980). Any conclusion about breed distribution should be made with reserva- tions but our data suggest that the buccal lymph node is mainly present in larger purebred dogs as no buccal lymph node was found in small or medium breeds or in the 41 mongrels examined in this study. The buccal lymph node is not only inconsistently found in dogs, but also in guinea pigs (Barone et al., 1950), primates and camels (Spira, 1962; Grau, 1974). In contrast, it is always present in humans and rabbits (Barone et al., 1950; Spira, 1962; Grau, 1974; Barone, 1996). Fig. 5a. Histological section of a canine buccal lymph node encapsulated The canine buccal lymph node is always located rostral by a capsule of dense connective tissue (C) sending trabeculae (T) into the to the masseter muscle and lateral to the buccinator mus- lymph node. The lymph node is composed of primary (I) and secondary cle, but its relation to the facial vein is variable. All canine (II) lymph follicles. A limited amount of adipose tissue (A) and erythrocytes (E) are scattered throughout the lymphoid tissue (Haema- buccal lymph nodes observed by Shelton and Forsythe toxylin-eosin staining). (1979) and Rumph et al. (1980) were located directly dorsal, ventral or rostral to the angle of confluence of the facial and superior labial veins. In addition to both studies, we have also observed two buccal lymph nodes which were located medial to these veins. Because of its localisation, the buccal lymph node could be confused with the accessory parotid or ventral buccal salivary gland. However, the identity of any presumed buccal lymph node can easily be determined histologically. Few data are available concerning the drainage area of the canine buccal lymph node. Afferent lymph from facial structures, including the nose, upper lip and buccal region, Fig. 5b. Histological section of a canine buccal lymph node containing drains into the buccal lymph nodes, and the efferent lymph- large clusters of adipose tissue (A) and a very limited amount of lymphoid tissue (L). The lymph node is encapsulated by a capsule of connective atics discharge into the mandibular lymph nodes (Shelton tissue (C) sending trabeculae into the lymph node (T) (Haematoxylin- and Forsythe, 1979). The drainage area of the canine buc- eosin staining). cal lymph node can be determined by injecting inert parti- C.R. Casteleyn et al. / The Veterinary Journal 175 (2008) 379–383 383 cles such as Chinese ink or Prussian blue (Barone, 1996) References into the connective tissue of various head regions of living dogs. The particles will then be captured by macrophages Adams, D.R., 1986. Canine Anatomy. first ed. Iowa State University which will enter the lymphatics and drain to the associated Press, Ames, pp. 394–395. Barone, R., 1996. Anatomie compareé des mammife`res domestiques, lymph nodes which will subsequently become stained. This Tome cinquie`me, Angiologie. Editions Vigot, Paris, pp. 695–697, 721– experiment would require a large number of animals 846. because of the low prevalence of the canine buccal lymph Barone, R., Bertrand, M., Desenclos, R., 1950. Recherches anatomiques node. Our findings would suggest that a minimum of 10 sur les ganglions lymphatiques des petits rongeurs de laboratoire. dogs of preferably large and pure breeds would be needed. Revue de Me´decine Ve´te´rinaire 101, 423–428. Evans, H.E., 1993. Miller’s Anatomy of the Dog. third ed. W.B. Saunders Company, Philadelphia, London, p. 726. 5. Conclusion Grasse´, P.-P., 1972. Traite´ de Zoo¨logie, Tome XVI, fascicule IV. Masson Editeurs, Paris, pp. 873–881. The canine buccal lymph node is clinically important as Grau, H., 1974. Vergleichende Darstellung des Lymphgefa¨ßsystems it can enlarge due to tumour metastasis or inflammation of der Saügetiere. Verlag Paul Parey, Berlin und Hamburg, pp. 5– the buccal region. In some diseased patients, however, the 12. Nomina Anatomica Veterinaria, 2005. 5th ed., World Association of swelling may remain idiopathic. Although the buccal Veterinary Anatomists, Hamburg, Columbia, Ghent, Sapporo, p. 109, lymph node is only present in a minority of dogs, clinicians 120. http://www.wava-amav.org (accessed 14.09.2006). should be aware of its existence when dealing with nodular Rumph, P.F., Garrett, P.D., Gray, B.W., 1980. Facial lymph nodes in buccal swelling in practice. dogs. Journal of the American Veterinary Medical Association 176, 342–344. Acknowledgements Shelton, M.E., Forsythe, W.B., 1979. Buccal lymph node in the dog. American Journal of Veterinary Research 40, 1638–1639. Spira, A., 1962. Die Lymphknotengruppen (Lymphocentra) bei den The authors are grateful to L. 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