(Suppl.), 165-179, 1994 the Lymphatics of Japanese Macaque

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Anthropol.Sci. 102(Suppl.), 165-179, 1994

The Lymphatics of Japanese Macaque

TOSHIYUKIHAYAKAWA FirstDepartment of Anatomy, The Jikei UniversitySchool of Medicine, Nishishinbashi,Minato-ku, Tokyo 105, Japan

ReceivedMay 6, 1993

Abstract There has been no anatomicalstudy on the lymphaticsystem of Japa nesemonkey.In the presentstudy, four Japanesemonkeys (Macaca fuscata fuscata, 2 males and 2 females) were studied on the lymphatic system injected with the Indian-ink.The jugular, subclavian, bronchomediastinaland lumbar lymphatic trunks were well demonstrated,but the intestinaltrunk was not fully revealedin this study. In this study the lymphaticsystem of Japanesemonkeys was compared with those of tree shrews,lemurs, marmosetsand rhesus monkeysusing the idea of Lymphocentrum(Lc), which was introducedby Baum (1930)and Grau (1943). It has been known that there are 15 Lc in tree shrews, 15 Lc in lemurs, 16 Lc in marmosets,and 16 or 18 Lc in rhesus monkeys.The present study showed 15 Lc including27 lymphnodes in Japanesemonkeys. It seems that the Japanesemon keyis rather more primitive than the rhesus monkey in the development of lymphatic system. Key Words: macaque, Japanese monkey, lymphatic system, comparative anatomy,lymphatics

INTRODUCTION Anatomy of the Japanese monkey has been limited to topographic and compara tivestudies. Studies of lymphatic system on the Japanese monkey have not been found available though there has been for the rhesus monkey, chimpanzee, gorilla, or baboon.

MATERIALS AND METHODS In the present study, four Japanese monkeys (Macaca fuscata fuscata, 2 males and 2 females) were used to investigate on the lymphatic system, injected with Indian- ink. After injection of the contrast material, the subjects were fixed with 10% neutral formaline for a few months. Then the subjects were studied by dissection using a stereomicroscope.

RESULTS The lymphatic vessels originating from the upper and lower lips, the eyelids and the face (Fig. 1) entered the submandibular lymph nodes (Fig. 2) after running along the anterior facial vein. The vessels from a part of the lower lip entered the 166 T. HAYAKAWA submental lymph nodes (Figs. 1 and 2) and the efferent vessels entered the submandibular lymph nodes. The lymphatic vessels from the auricles entered the parotid lymph nodes (Fig. 2). The efferent vessels from the submandibular, submental and parotid lymph nodes ran independently and entered the superficial cervical lymph nodes (Fig. 2), which were located near the junction of the external jugular and the anterior facial veins. The superficial cervical lymph nodes were one of the terminal lymph nodes in the head and neck. Another terminal lymph node was the cranial deep cervical lymph node (Fig. 3), which received the lymphatic vessels from the tongue. The efferent vessels from these two terminal lymph nodes coursed together to make the jugular lymphatic trunk running to the venous angle. There were two lymphatic routes in the fore-limb. The routes arose from the subcutaneous lymphatic network extending from back of the hand to the wrist joint. Firstly, the lymphatic vessels from this network proceeded in the anterior aspect of the fore-arm along the antebrachial cephalic and median veins and subcutaneous branches of nerves to the elbow joint. In the upper arm, they proceeded along the cephalic vein and became four or five streaks (Fig. 4). They entered the superficial axillary lymph nodes (Figs. 2, 3, and 5) near the quadrangular space of the shoulder joint region and finally reached the deep axillary lymph nodes (Fig. 5). Secondly, some of lymphatic vessels from the lymphatic network in the hand inclined toward the ulnar side in the anterior aspect of fore-arm and proceeded along the basilic vein in the upper arm. This route directly entered the deep axillary lymph nodes (Fig. 5). The deep axillary lymph nodes also received subcutaneous lymphatic vessels of the thorax (Figs. 1, 2, 4 and 5). The efferent vessel of the deep axillary lymph nodes was the subclavian lymphatic trunk. The trunk proceeded along the lateral thoracic artery and vein in turn. After extending a communicating vessel to the jugular trunk, it entered the vein at the merging point of the external jugular and the subclavian vein. The left subclavian trunk ran together with the left jugular trunk and the thoracic duct (Fig. 3). The ventral route of the lymphatic vessels from the diaphragm, the intercostal space and the heart terminated in the anterior superior mediastinal lymph nodes (Figs. 6 and 7). The dorsal route from these areas mainly entered the thoracic duct (Figs. 12 and 17). The draining pathways in the lung were very complicated. A part of vessels from the right and left lungs proceeded behind the both bronchi and entered the bifurcational lymph nodes at the bifurcation of the trachea (Fig. 8). The efferent vessel of the this lymph node entered the left tracheobronchial lymph nodes. The lymphatic vessels from the left tracheobronchial lymph nodes entered the brachiocephalic venous angle lymph nodes via the paratracheal and pretracheal lymph nodes. The lymphatic vessels of the right lung entered mainly the right mediastinal lymph node via the paratracheal and tracheobronchial lymph nodes. The efferent vessels from the two terminal lymph nodes made a form of the The Lymphatics of Japanese Macaque 167

Figs. 1, 2 and 3. The lymphatic system in the head and chest. DAL, deep axillary lymph node; DCL, deep cervical lymph node; PL, parotid lymph node; SAL, superficial axillary lymph node; SCL, superficial cervical lymph node; SML, submandibular lymph node; SUL, submental lymph node; JLT, jugular lymphatic trunk; SLT, subclavian lymphatic trunk; TD, thoracic duct; a, auricle; afv, anterior facial vein; dm, deltoid muscle; e, eyelid; ejv, external jugular vein; gpm, great pectral muscle; 11,lower lip; mg, mammary gland; n, nose; pg, parotid gland; sb, sternal bone; t, trachea; ul, upper lip. 168 T. HAYAKAWA

Figs. 4 and 5. The superficial (Fig. 4) and deep (Fig. 5) lymphatic pathway in the foreleg. acv, antebrachial cephalic vein; bv, basilic vein. bronchomediastinal lymphatic trunk. In these subjects, the trunk was observed in all the cases on the right but none on the left (Fig. 8). The lymphatic vessels from the stomach ran parallel with the left gastric artery and entered the left gastric lymph nodes. This lymph node received the lymphatic vessels from the spleen via the splenic lymph nodes. The hepatic lymph node accepted the lymphatic vessels originating from the liver, and received a part of the lymphatic vessels from the pancreas, duodenum, and pylorus of the stomach via the pancreaticoduodenal lymph nodes (Fig. 9). These lymph nodes belonged to a group The Lymphatics of Japanese Macaque 169

Figs. 6, 7 and 8. The lymphatic system of thorax. ASL, anterior superior mediastinal lymph node; BL, bifurcational lymph node; BLT, bronchomediastinal lymph trunk; BVL, bracheocephalic venous angle lymph node; PRL, pretracheal lymph node; PTL, paratracheal lymph node; RLT, right lymphatic trunk; SLT, subclavian lymphatic trunk; TD, thoracic duct; TL, tracheobronchial lymph node; b, bronchus; d, diaphragm; es, esophagus; h, heart; k, kidney; lu, lung; t, trachea; *, the ventral route of the lymphatic vessel from the diaphragm(d). 170 T. HAYAKAWA of the celiac lymph nodes. The lymphatic vessels from the small intestine and colon were collected by the mesenteric lymph nodes (Fig. 10), and entered the lymphatic vessels from the sigmoid colon and rectum. A part of the lymphatic vessels from the colon and rectum supplied by the inferior mesenteric artery en teredthe mesocolic lymph nodes. The efferent vessels from this lymph node entered the pubic lymph node and sacral lymph node. The lymphatic vessels from the kidney arose at its hilum and entered the renal lymph node which was located near the root of the renal artery. The efferent vessels from this lymph node entered the left paraaortic lymph node or right paravenosus lymph node (Figs. 11 and 12). The lymphatic vessels from the bladder entered the sacral lymph node through the iliac lymph nodes (Fig. 13). The lymphatic vessels from the testicular or ovar ianorgan entered the superior lumbar lymph nodes (paraaortic, interaorticovenous and paravenousus lymph nodes), and received 2 or 3 streaks of lymphatic vessels running along the testicular and ovarian artery and vein from the respective organs (Fig. 14). The lymphatic vessels from the glans penis or the perineum had two lymphatic routes in the external genital organ. Firstly, the lymphatic vessels of the subcutaneous lymphatic network entered the superficial inguinal lymph nodes (Figs. 15 and 19). Secondly, deep lymphatic vessels in those organs entered the superior lumbar lymph node (Fig. 16). The paraaortic lymph nodes and paravenousus lymph nodes by the abdominal aorta were the final lymph nodes of the lymph vessels from the hind legs, tail, perineum, and pelvis. The efferent vessels from these nodes formed the lumbar lymphatic trunk (Figs. 17 and 18). The lymphatic vessels from the organs supplied by the celiac trunk were collected by a group of celiac lymph nodes composed of the left gastric, hepatic, splenic and pancreaticodoudenal lymph nodes. On the other hand, the lymphatic vessels from the organs supplied by the superior mesenteric artery entered the mesenteric lymph nodes. These were two lymphatic vessels; one entered the cisterna chyli via celiac lymph nodes and the other entered directly the cisterna chyli. These findings suggest that the intestinal lymphatic trunk may not be complete in this species (Fig. 18). The lymphatic network from the subcutaneous in the hind legs observed two routes. The superficial lymphatic vessels originating from the network entered the superficial inguinal lymph nodes (Fig. 19) in the tight triangle. The deep lymphatic vessels from the network extending from the toes to the ankle ascended with the small saphenous vein and entered the popliteal lymph node (Fig. 20). The efferent vessels from this node ran parallel with the sciatic artery and vein and entered the iliac lymph nodes (Fig. 20). The thoracic duct originated at the first to third lumbar vertebras from the cisterna chyli which was the union of the left and right lumbar trunks (Figs. 17 and 18). The thoracic duct ascended on the right dorsal side of the abdominal aorta and reached the thoracic region after penetrating the aortic hiatus. In the thoracic region, it The Lymphatics of Japanese Macaque 171

Figs. 9, 10 and 11. The visceral and parietal lymphatic system in abdomen. HL, hepatic lymph node; LGL, left gastric lymph node; ML, mesenteric lymph node; MCL, mesocolic lymph node; PDL, pancreaticoduodenal lymph node; PVL, paravenousus lymph node; RL, renal lymph node; SL, splenic lymph node, co, colon; ct, celiac trunk; du, duodenum; gb, gall bladder; ivc, inferior vena cava; k, kidney; li, liver; pa, pancreas; pv, portal vein; s, stomach; sc, sigmoid colon; si, small intestine; sma, superior mesenteric artery; sp, spleen. 172 T. HAYAKAWA

ascended along the right outer surface of the thoracic aorta and turned to the left at the 5th or 6th thoracic vertebra. Further it ascended between the left common carotid and subclavian arteries to the level near the superior thoracic aperture and drained into the vein at the angle of union of the internal jugular and subclavian veins after merging with the left jugular and subclavian lymphatic trunks (Figs. 3 and 8). The right lymphatic trunk formed a common vessel near the junction of the venous angle from the jugular, subclavian and bronchomediastinal lymphatic trunks.0 The right lymphatic trunk may not be complete in this species (Figs. 6 and 8).

DISCUSSION The sites where the lymph nodes appear are generally constant within the same species and the individual difference is small (Kutsuna, 1968). In the lower mam-

Figs. 12, 13, 14 and 15. Main lymph flow in the posterior abdominal wall (Figs. 12 and 13). The uperficial and deep lymphatic pathway male genital organ (Figs. 14 sand 15). IL, iliac lymph node; MCL, mesocolic lymph node; PAL, paraaortic lymph The Lymphatics of Japanese Macaque 173 mals, such as bats (Hayakawa, 1981a) and moles (Hayakawa, 1981b), the sites and the number of lymph nodes were reported. In dealing with the difference of spe cies,it is useful to introduce the idea of lymphocentrum (Lc) by Baum (1930) and Grau (1943). Concerning the lymphatic systems of various mammals, Spira (1962) made comparison using this idea. In the present study, the lymphatic system of the Japanese monkey was compared with those of Lemur macaco (Teshima, 1936), Tupaia (Sasaki, 1984), Callithrix penicillata (DiDio et al., 1959), and Macaca mulatta (Teshima, 1936) (Table 1). Lemurs and tree shrews have 15 Lc and mar mosetshave 16 Lc. On rhesus monkeys, 16 Lc are identified by Teshima (1936), but 18 Lc by Endo (1941). The present study showed 15 Lc including 27 lymph nodes in Japanese monkeys (Table 1). The number of the common Lc in these five species including the Japanese monkey, is 12. Comparing the number of lymph nodes with the same Lc, it is clear that tree shrew and lemur are evolutionally

node (PVL, paravenosus lymph node); PUL, public lymph node; SCL, sacral lymph node; SIL, superficial inguinal lymph node; aa, abdominal aorta; cia, common iliac artery; ima, inferior mesenteric artery; p, penis; ra, renal artery; srg, suprarenal gland; st, scrotum; tt, testis; u, ureter; ub, urinary bladder; *, the dorsal route of the lymphatic vessel from the diaphragm(d). 174 T. HAYAKAWA

Figs. 16, 17 and 18. Main lymph flow in the abdominal and pelvic organs. CL, celiac lymph node; IAL, interaorticovenous lymph node; LLT, lumbar lymphatic trunk, CC, cisterna chyli. The Lymphatics of Japanese Macaque 175

Figs. 19 and 20. The superficial and deep lymphatic pathway in the hindleg. POL, popliteal lymph node. 176 T. HAYAKAWA

Table 1. Comparison of lymph nodes belonging to various lymphocentra The Lymphatics of Japanese Macaque 177

Table 1. (cont'd)

1) Lemur macaco: Teshima (1935), 2) Callitherix penicillata: Didio et al. (1959), 3) Macaca mulatta: Teshima (1936), 4) Macaca mulatta: Endo (1941), 5) Tupaia: Sasaki (1984) 178 T. HAYAKAWA lower than mamoset and rhesus monkey. This result also indicates that tree shrew is the useful subject for exploring fundamental structure of the lymphatic system in primates. The intestinal trunk of Japanese monkey was made by the union of the efferent vessels of the mesocolic and mesenteric lymph nodes like that or rhesus monkey. But the existence of the other direct route from the mesenteric lymph nodes to the lumbar trunk indicates that the intestinal trunk in this species is incomplete. In general, the lumbar trunk is the efferent vessel of the lumbar lymph node and lies outside the abdominal aorta or vena cava inferior. Teshima (1936) distin guishedthe cranial from caudal aortic lymph node in rhesus monkey. He described that the efferent vessel of the cranial aortic lymph node was the lumbar trunk. The cranial and caudal lymph nodes were also distinguished in lower mammals, such as moles (Hayakawa, 1981a) and rats (Seo, 1981). However, such distinction was not found in lemur (Teshima, 1936) and tree shrew (Sasaki, 1987). In the Japanese monkey, the efferent vessels from the paraaortic lymph node and paravenousus nodes formed the lumbar lymphatic trunk. The final lymph node which the jugular trunk gave rise to in rhesus monkey and lemur was the inferior deep cervical lymph node. On the other hand, the final lymph node in mole was the superior deep cervical lymph node. As mentioned in the results, the final lymph nodes in Japanese monkey were in the superficial cervical and the superior deep cervical regions as in tree shrew. Lemur and tree shrew belong to the same suborder, the prosimii, but the final lymph node in the cervical region was different between them. To the contrary, those in mole and tree shrew are similar to each other, despite they are of different orders. The final lymph node to the subclavian trunk was the superior axillary lymph node in rhesus monkey, the axillary lymph node in lemur, the deep axillary lymph node in tree shrew, mole and Japanese monkey. Although their names are different, their locations are similar. The final lymph node to the lumbar trunk was the cranial aortic one in rhesus monkey. This lymph node located more cranially than the caudal aortic node in this species. The lymph node is aortic lymph node in lemur (Teshima, 1936), and paraaortic lymph node in mole (Hayakawa, 1981a), tree shrew (Sasaki, 1984) and Japanese monkey. Teshima (1936) did not refer to the bronchomediastinal lymphatic trunk of rhe susmonkey. Usually the trunk is not formed in the human. On the contrary, it was frequently observed in the lower mammals, such as rats, bats, and moles. In Japa nesemonkey and tree shrews, it was 100% on the right side, and none on the left side. In rhesus monkey, the intestinal trunk was made by the union of the efferent vessels from the mesocolic and mesenteric lymph nodes, and it entered the cisterna chyli. In moles, it was made by the union of the efferent vessels of the celiac and The Lymphatics of Japanese Macaque 179 mesenteric lymph node, and also entered the cisterna chyli. In lemur, two streaks of short intestinal trunk arose from the mesenteric lymph node and entered the tho racicduct. It seems that the Japanese monkey is rather more primitive than the rhesus monkey in the development of the lymphatic system. Consequently, the author suggests that the fundamental pattern of the lymphatic system in Japanese monkey situated at the position linking the primitive primates with the higher primates.

ACKNOWLEDGEMENTS The author wishes to express his gratitude to Prof. H. Yamashita and Assist. Prof. S. Kato for their valuable comments on this work. English was contributed by Dr. I. Kageyama. Thanks are also due to the staff of the First Dept. of Anat. for their encouragements.

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