Okajimas Fol. anat. jap., 42: 265-280, 1966.

Stereological Studies on Several Ducts and Vessels by Injection Method of Acrylic Resin

XVI. Arterial Distribution of the Submandibular Lymph Nodes in Some Mammals

By

T. Miyata

Department of Anatomy, Osaka Dental College, Osaka (Director : Prof. Y. Taniguchi) (With 33 figures in 4 plates)

This work was announced at the 67th Annual Session of the Japanese Association of Anatomists, 1962, Kurume.

Preface The author has observed comparatively the arterial distribution of the submandibular lymph nodes in some mammals. Lymph node branches and their resources have been studied by means of the_ stereological approach. This survey was undertaken to observe the arterial supply to the lymph nodes and to observe which arterial supply is the main route.

Materials and Methods

Animals used : 24 dogs, 26 cats, 21 rabbits, 13 goats and 22 human fetuses (6-10 months). Plastics injection was applied by method of Tani g u c h i, 0 h t a and T a jiri (1952 and 1955). The material was injected through. cannulae inserted into the common carotid . Observations. and dissections were made on corrosion specimens and the acrylic- injected 10% formalin-preserved specimens under binocular magni- fier.

265 266 T. Miyata

Observations

I. Distributing arteries _Dog: Distributing arteries are five : (1) R. in. submandibularis of the facial, (2) of the external carotid, (3) of the posterior auricular, (4) of the superior thyroid and (5) of the maxillary . Of them, one to three in number supply the nodes in each case : only (2) in 6 cases of 24 examples, (1) and (3) in 4 cases, (1) and (2) in 5 cases, (1), (2) and (4) in 1 case, only (3) in 3 cases, (3) and (4) _in 2 cases, (1) and (5) in one case, and (1), (3) and (4) in 2 cases. (1) R. ln. submandibularis of the (13 cases) (Figs. -5-7). The ramus (0.19-0.48, M. 0.32 mm) arises from the inferior wall of the facial behind the anterior margin of the masseter muscle. It leaves the beginning of the in three cases. It ...arches backward after branching forward and passes to the nodes -under the platysma . (2) R. ln. submandibularis of the (12 -cases) (Figs. 1, 2, 3 and 9.) The ramus (0.49-0.75, M. 0.62 mm) arises from the posterior wall of the external carotid, 1-5 mm distal to the beginning of the pos- terior auricular, medial to the and infrapos- -bterior to the masseter muscle. In one case, it leaves the parotid ranch of the artery (Fig. 3). The ramus passes anterolaterally up to between the masseter and the supranterior margin of the submandibular gland. Then, it comes onto the lateral surface of the masseter and to the nodes meanderingly or rotatingly (Fig. 9). (3) R. ln. submandibularis of the posterior auricular artery (11 cases) (Figs. 4-7). The ramus (0.49-0.93, M. 0.70 mm) arises from the superior wall of the posterior auricular about 1.5 mm distal to the beginning of It. The ramus just follows the course of the branch (2). (4) R. ln. submandibularis of the (5 .cases) (Figs . 5, 7 and 8). The ramus (0.37-0.62, M. 0.49 mm) arises from branches to the sternohyoideus and the sternothyreoideus at the lateral side of the cricothyreoideus. It passes laterally to the nodes on the sterno- hyoideus and the digastricus. Arterial Distribution of Submandibular Lymph Nodes in Some Mammals 267

(5) R. In. submandibularis of the (one case). The ramus (0.48 mm) arises from the superior wall of the maxil- lary close to its beginning in the retromandibular region. It passes anterolaterally onto the lateral surface of the masseter muscle and reaches the nodes downward.

Cat : Distributing arteries are four : (1) R. ln. submandibularis of the facial, (2) of the posterior auricular, (3) of the external carotid and (4) of the superficial temporal artery. Of them, one to three in number are observed in each case : (1) and (2) in 10 cases of 26 examples, only (2) in 2 cases, (1) and (3) in 2 cases, only (1) in 4 cases, (2) and (3) in 4 cases, only (3) in 2 cases, (1), (2) and (3) in one case, and (1), (3) and (4) in one case. (1) R. ln. submandibularis of the facial artery (18 cases) (Figs. 10-12). The ramus (0.17-0.46, M. 0.27 mm) arises from any walls of the facial between beginnings of the submental and of the inferior labial in 11 cases, and 1-2.5 mm distal to the beginning of the in- ferior labial in 3 cases. But, it is observed as a twig of the sub- mandibular glandular branch (T a k a shim a, 1962) of the artery in 3 cases (Fig. 11) and as of the masseter branch in one case. It, passes infraposteriorly to the nodes along inferior to the digastricus tortuously. (2) R. ln. submandibularis of the posterior auricular artery (17 cases) (Figs. 12 and 13). The ramus (0.24-0.60, M. 0.36 mm) arises from the superior, anterior or posterior wall of the posterior auricular, at the antero- medial end of the submandibular gland and the superior margin of the digastricus. It runs anterolaterally between the parotid and the submandibular glands (Fig. 12), giving twigs to them, up to the nodes. (3) Rr. inn. submandibulares of the external carotid artery (10 cases) (Figs. 13 and 14). (i) In case of arising proximal to the beginning of the lingual (8 cases) (Fig. 13). The ramus (0.24-0.41, M. 0.34 mm) arises from the superior or infranterior wall of the external carotid, about 3.5 mm medial to the beginning of the lingual. It leaves for the supraposterior, and immediately turns forward at the infraposterior end of the sub- mandibular gland up to the medial nodes. 268 T. Miyata

(ii) In case of arising distal to the beginning of the posterior auricular (2 cases) (Fig. 14). The rami (0.29-0.41, M. 0.36 mm), two in number, arise from the anterior or lateral wall of the external carotid, 0.5-3.7 mm distal to the beginning of the posterior auricular. They follow the course of the node branch of the posterior auricular. (4) R. in. submandibularis of the superficial temporal artery (one case) (Fig. 15). The ramus (0.29 mm) arises from the posterior wall of the super- ficial temporal, about 1.5 mm distal to its beginning. It breaks into two which pass infranteriorly to the nodes meanderingly. Rabbit : Distributing arteries are three : (1) R. in. submandibularis of the submental, (2) of the facial and (3) of R. massetericus of the facial artery. Of them, one in number is observed in each case : only (1) in 12 cases of 21 examples, only (2) in 8 cases, and only (3) in one case. (1) R. ln. submandibularis of the submental artery (12 cases) (Figs. 16 and 18). End (0.36-0.96, M. 0.61 mm) of the submental in 5 cases runs forward along the superior margin of the digastricus, giving twigs to it, up to its insertion, where it turns backward to the nodes. The ramus (0.24-0.41, M. 0.32 mm) arises from the inferior wall, right after the beginning of the submental in 7 cases. It passes medially to the nodes meandringly along the facial artery. (2) R. ln. submandibularis of the facial artery (8 cases) (Figs. 17-19). The ramus (0.26-0.36, M. 0.32 mm) arises from the medial wall of the facial at the mandibular basis. It passes infraposteriorly along the facial for 6-9 mm distant, tortuously or rotatingly up to the beginning of the submental, where it turns forward to the nodes. (3) R. in. submandibularis of R. massetericus of the facial artery (one case) (Fig. 20). The ramus (0.29 mm) arises from the medial wall of the mas- setericus. It first runs backward, then forward along the infra- lateral margin of the submandibular gland and the facial artery up to the nodes. Arterial Distribution of Submandibular Lymph Nodes in Some Mammals 2e&

Goat : Distributing arteries are two : (1) R. ln. submandibularis of R. facialis of the lingual or (2) of the in 13 examples. (1) R. ln. submandibularis of R. facialis (0 k a n o, 1960) of the lingual artery (9 cases) (Figs. 21-23). The ramus (0.29-0.79, M. 0.50 mm) arises from any walls of R. facialis of the lingual. It runs backward abreast with the facial vein, and turns forward on the infralateral margin of the sub- mandibular gland up to the nodes. (2) R. ln. submandibularis of the lingual artery (4 cases) (Figs. 24 and 25). The ramus (0.34-0.55, M. 0.44 mm) arises from the inferior wall of the lingual, 3-6 mm distal to the beginning of the R. gl. sub- mandibularis (T a k a s h i m a 1962). It runs infraposteriorly to the nodes along the digastricus and the submental vein meanderingly or rotatingly. Human fetus : Distributing arteries are three : (1) R. ln. submandibularis of R. massetericus of the facial, (2) of the facial and (3) of the submental artery. Of them, one to three in number are observed in each case : (1), (2) and (3) in 7 cases of 22 examples, (1) and (3) in 6 cases, (1) and (2) in 4 cases, (2) and (3) in 3 cases and only (2) in 2 cases. (1) Rr. Inn. submandibulares of R. massetericus of the facial artery (17 cases) (Figs. 28-33). The rami (0.12-0.22, M. 0.17 mm), three in number in three cases, arise from the anterior or posterior wall of the massetericus of the facial, 0.4-5.5 mm distal to its beginning. They pass forward along the mandibular basis, sometimes making loops, up to the nodes. (2) Rr. inn. submandibulares of the facial artery (16 cases) (Figs. 27-31). The rami (0.12-0.38, M. 0.18 mm), two in number in five cases, arise from the anterior wall of the facial, 0.5-5.2 mm distal to the submental. They pass infranteriorly along the mandibular basis, sometimes recurring after running backward along the facial, up to the nodes, giving off cutaneous twigs. (3) R. ln. submandibularis of the submental artery (16 cases) (Figs. 27 and 31-33). The ramus (0.07-0.26, M. 0.17 mm) arises from the inferior or lateral wall of the submental, 2.0-13.5 mm distal to its beginning. 270 T. Miyata

It immediately passes backward between the facial and the sub- mental arteries up to the nodes.

II. Features of R. in. submandibularis In all species observed, entrance views of the lymph node branches are extremely complex, that is, according to numbers of the resource and the node. The branches in general break into small twigs meanderingly or rotatingly, and which communicate with those out of other resources when they come close to the nodes. Dog and Cat : In dog, the nodes are one to four in number ; two are observed in 12 cases of 24 examples, three in 7 cases, 4 in 4 cases and one in one case. Number of the supply resources is two in 12 cases, one in 9 cases, and three in three cases. In cat, the nodes are one to three in number ; two are observed in 21 cases of 26 examples, one in three cases and three in two cases. Number of the supply resources is two in 15 cases, one in 8 cases and three in three cases. The nodes of both species are located mediolaterally. Rabbit : The nodes are one in number in 12 cases of 21 examples and 2 in 9 cases. They in all cases are supplied with only one source. They are located anteroposteriorly.

Goat : The node is only one in all 13 examples. Human fetus : The nodes are 3 in number in 12 cases of 22 examples, 2 in 7 cases, 4 in 2 cases and one in one case. Number of the supply resources is 2 in 13 cases, 3 in 7 cases and one in 2 cases. They are located anteroposteriorly. In all species, the node branch enters the nodes in the following features :— (1) In case of one node : If the node has two supply resources, each branch of them enters the node from anterior and posterior sides. (2) In case of two nodes : The branch breaks into four, and each two of which enter Arterial Distribution of Submandibular Lymph Nodes in Some Mammals 271

each node. Or, one branch enters the lateral or anterior node and the other branch out of the other resource does the medial or posterior node after anastomosing with the first branch. Or , each. node is supplied with each resource . (3) In case of three nodes : The lateral or anterior node is supplied with the branch out of one resource, the middle one with a communication between it and a branch of the other resource which supplies the medial or posteri- or node. (4) In case of four nodes : The lateralmost or anteriormost and the middle two nodes are- supplied with a branch of one resource, while the medialmost or- posteriormost with a branch of the other resource.

Discussion Comparative views of the distributing arteries were made into a table. It was summarized that the main arterial supply was the. R. ln. submandibularis of the facial artery and its branches, but in goat, of the lingual and its branches.

1. R. ln. submandibularis of the facial artery or its branches. The ramus was the main distributing artery in dog, cat, rabbit and human fetus. Ellenberger et al. (1891) stated that twigs to the submandi- bular lymph nodes were given from the facial when the artery passed between the digastricus and the masseter in dog. H U r I i- m a n n (1912) stated that small twigs diverged from the facial to the nodes in cat. It was ascertained that actual features of the ramus were more_ complex than in the previous observations. Additionally, the lymph. node branch arose from the beginning of the inferior labial or near it. The branch also arose from the R. gl. submandibularis of the. facial. And, when the branch bifurcated, the lateral and medial nodes. were supplied with each one in usual cases. But, when the branch, did not break into, it entered at first the medial node and then the. lateral one. In rabbit, the node branch usually left the artery in its. facial portion, showed meandering or loop-forming, and usually one resource supplied one lymph node. In human fetus, the node branches were not longer than those in other animals observed. 272 T. Miyata

2. R. ln. submandibularis of the external carotid or the posterior auricular arteries. Rami of these arteries were observed in dog and cat, but not main supply branches. In dog, the node branch from the external carotid left distal to the beginning of the posterior auricular. In cat, the branch left the external carotid proximal to the beginning of the lingual or distal to the beginning of the posterior auricular. In both species, the branch from the posterior auricular left near its origin. In cases of which were supplied with these two resources in dog, the larger branch usually supplied the medial lymph node, and the smaller did the lateral one. In cat, the branch from the posterior auricular usually entered the lateral node, even if the nodes were two or more. In two cases, node branches of which had two origins in the external carotid, and the branch from distal to the beginning of the posterior auricular supplied the lateral node, and the other from proximal to the beginning of the lingual did the medial one.

3. R. ln. submandibularis of the submental artery. The ramus was observed in rabbit and human fetus. It was the -main arterial supply in the former , and it in the latter left the mus- cular branch of the submental. Si c her (1952) stated in his textbook the submental artery supplied the submandibular lymph node. In the present paper, the branch of the artery usually entered the anterior lymph nodes. In rabbit, end or branch of the submental entered the lymph nodes. End of it usually was long and took a recurrent course to supply nodes after giving many twigs to the digastricus. Branch -en route of it usually showed a loop-forming. On the contrary -Mi , y a t a et al. (1965) observed in guinea pig the node branch of the artery was shorter and took simple courses.

.4. R. ln. submandibularis of R. massetericus of the facial artery. The ramus was observed in human fetus and rabbit. It was the main arterial resource in human fetus, and usually entered the pos- terior nodes. In one case of rabbit, in which this ramus was observed, -it might take the place of the node branch of the facial .

.5. R. ln. submandibularis of the superior thyroid artery . Miller (1964) stated in dog that the submandibular lymph nodes were supplied with the muscular branch of the cranial thyroid artery. The present author also observed the node branch of the artery only in dog. Arterial Distribution of Submandibular Lymph Nodes in Some Mammals 273

6. R. ln. submandibularis of the lingual artery. The ramus was the one and only in goat. The node branch left the lingual or the R. facials which was in place of the facial.

7. R. ln. submandibularis of the maxillary or the superficial temporal arteries. The ramus of the maxillary was observed in one case of dog. It might be a variation of the ramus of the posterior auricular, because it showed almost the same course with the ramus. The ramus of the superficial temporal was observed in one case of cat. It also might be a variation of the ramus of the posterior auricular for the above reason.

Table

0 Main arterial supply. 0 Supplemental arterial supply. Number in each mark shows a frequency order.

Conclusions 1. Comparative observations were made by the acrylic resin in- jection method on the arterial distribution of the submandibular lymph nodes, especially, the arising aspect from arterial resources and the entrance view into the nodes in dog, cat, rabbit, goat and human fetus. 2. In dog, cat, rabbit and human fetus, the submandibular lymph node branches of the facial, the submental and their branches were observed almost in all cases. 274 T. Miyata

3. In dog and cat, the node branches of the external carotid and the posterior auricular arteries were strong in all cases observed. 4. In goat, the node branches arose from the lingual artery and its branches. 5. The node branches of the superior thyroid and the maxillary arteries in dog and of the superficial temporal artery in cat were rarely observed. 6. One node was commonly supplied with more than two resources in dog, cat and human fetus. One node branch supplied commonly one node in goat and rabbit.

The author should like to express his thanks to Professor Y. Taniguchi for guidance and encouragement shown to him, and also to Assistant Professor Y. 0 ht a for his help in surveying spe- cimens and preparing the manuscript.

Literature Cited

1) Elle n b e r g e r, W. and H. B a u m, 1891. Systematische und topographische Anatomie des Hundes. Berlin, 51 : 376-385. 2) H u rlim an n, R. 1912. Die arteriellen Kopfgefasse der Katze. Intern. Mschr. Anat., 29 : 397-399. 3) Mille r, M. E. 1952. Guide to the dissections of dog. W. S. Saunders Co., Phila- delphia, 267-388. 4) Miy at a, T., K. Kamakura and S. Ka nek o, 1965. Distributing arterial branches of the submandibular lymph nodes in guinea pig. Okajimas Fol. anat. jap., 41 : 221-223. 5) 0 k a n o, H. 1960. On the ramification of A. lingualis and its fine distribution in some mammals. Okajimas Fol. anat. jap., 37: 204-206. 6) Si c h e r, H. 1952. Oral anatomy. C. V. Mosby Co., 3rd ed., Saint Louis, 315-354. 7) T a k a s h i m a, T. 1962. Arterial branches supplying the submandibular gland in some mammals. Abstract of the 67th Annual Session of the Japanese Association of Anatomists, 1962, Kurume. . 8) Taniguchi, Y., Y. Ohta and S. Tajiri, 1952. New improved method for injection of acrylic resin. Okajimas Fol. anat. jap., 24: 259-267. 9) Taniguchi, Y., Y. Ohta, S. Tajiri, H. Okano and H. Hanai, 1955. Sup- plement to new improved method for injection of acrylic resin. Okajimas Fol. anat. jap., 27 : 401-406. Arterial Distribution of Submandibular Lymph Nodes in Some Mammals 275

Explanation of Figures

Abbreviations

L submandibular lymph node M mandibule Gm submandibular gland f facial artery fm R. massetericus of facial artery s submental artery x R. ln. submandibularis e external carotid artery m maxillary artery th superior thyroid artery pa posterior auricular artery t superficial temporal artery 1 lingual artery If R. facialis of lingual artery direction of nares

Plate I Figs. 1-9. Dog. Fig. 1. R. ln. submandibularis of the external carotid artery. c. 1. 4 x . Figs. 2. and 3. R. in. submandibularis of the external carotid artery supplies two lymph nodes. c. 1.8 x. Fig. 4. R. ln. submandibularis of the posterior auricular artery. c. 1. 4 x. Fig. 5. R. In. submandibularis of the posterior auricular artery supplies one node, and rami of the superior thyroid and the facial arteries do the other. c. 1.8 x. Fig. 6. Rr. Inn. submandibulares of the posterior auricular and the facial arteries supply a node. c. 1.8 x. Fig. 7. R. in. submandibularis of the posterior auricular artery supplies one node, and rami of the facial and the superior thyroid arteries do the other. c. 1. 2. x. Fig. 8. R. ln. submandibularis of the superior thyroid artery. c. 1.2 x. Fig. 9. Close-up of two nodes. c. 2.7 x.

Plate II Figs. 10-15. Cat. Figs. 16 and 17. Rabbit. Fig. 10. R. ln. submandibularis of the facial artery. c. 2 x . Fig. 11. R. In. submandibularis of the submandibular glandular branch of the facial artery. c. 2.5 x. Fig. 12. Rr. Inn. submandibulares of the facial and the posterior auricular arteries. c. 1.4 x . Fig. 13. Rr. Inn. submandibulares of the posterior auricular and the external carotid arteries. c. 1.6 x. Fig. 14. Two Rr. Inn. submandibulares of the external carotid artery supply one node. c. 1. 8 x . Fig. 15. R. ln. submandibularis of the superficial temporal artery. c. 1.8 x. 276 T. Miyata

Fig. 16. R. ln. submandibularis of the submental artery supplies two lymph nodes . c. 2.8 x . Fig. 17. R. ln. submandibularis of the facial artery supplies two lymph nodes. c. 2.5 x.

Plate III Figs. 18-20. Rabbit. Figs. 21-25. Goat. Fig. 18. Rr. Inn. submandibulares of the facial and the submental arteries. c. 1.6 x . Fig. 19. R. ln. submandibularis of the facial artery. c. 2 x Fig. 20. R. In. submandibularis of R. massetericus of the facial artery. c. 2.3 x. Figs. 21-23. R. ln. submandibularis of R. facialis of the lingual artery. c. 1.8 x. Figs. 24 and 25. R. ln. submandibularis of the lingual artery. c. 1.3 x.

Plate IV Figs. 26-33. Human fetus. Fig. 26. Three nodes of the right side. c. 1. 8 x. Fig. 27. R. In. submandibularis of the facial artery supplies three nodes, and one of them is supplied with R. In. submandibularis of the submental artery. c. 2 x. Fig. 28. Two nodes are supplied with R. In. submandibularis of the facial artery, and the other with R. In. submandibularis of R. massetericus of the external carotid artery. c. 2 x. Figs. 29 and 30. •Rr. inn. submandibulares of the facial artery and R. massetericus of it. c. 2 x Fig. 31. Each R. ln. submandibularis of the facial and the submental arteries and of R. massetericus of the facial artery supplies one node, respectively. c. 2 x. Fig. 32. Ir. Inn. submandibulares of the submental artery and of R. massetericus of it. c. 1.6 x - Fig. 33. R. In. submandibularis of the submental artery supplies two nodes, and of R. massetericus of the facial artery does the other. c. 2 x. Arterial Distribution of Submandibular Lymph Nodes in Some Mammals Plate I

T. Miyata Arterial Distribution of Submandibular Lymph Nodes in Some Mammals Plate II

T. Miyata Arterial Distribution of Submandibular Lymph Nodes in Some Mammals Plate III

T. Miyata Arterial Distribution of Submandibular Lymph Nodes in Some Mammals Plate IV

T. Miyata