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

The Lymphatics of Japanese Macaque

TOSHIYUKI HAYAKAWAFirst Department of Anatomy, The Jikei University School of Medicine,

Nishishinbashi, Minato-ku, Tokyo 105, Japan

Received May 6, 1993

Abstract There has been no anatomical study on the lymphatic system of Japanesemonkey. In the present study, four Japanese monkeys (Macaca fuscata fuscata,2 males and 2 females) were studied on the lymphatic system injected with theIndian-ink. The jugular, subclavian, bronchomediastinal and lumbar lymphatictrunks were well demonstrated, but the intestinal trunk was not fully revealed inthis study. In this study the lymphatic system of Japanese monkeys was comparedwith those of tree shrews, lemurs, marmosets and rhesus monkeys using the ideaof Lymphocentrum (Lc), which was introduced by Baum (1930) and Grau (1943).It has been known that there are 15 Lc in tree shrews, 15 Lc in lemurs, 16 Lc inmarmosets, and 16 or 18 Lc in rhesus monkeys. The present study showed 15 Lcincluding 27 lymph nodes in Japanese monkeys. It seems that the Japanese monkeyis rather more primitive than the rhesus monkey in the development oflymphatic system.

Key Words: macaque, Japanese monkey, lymphatic system, comparativeanatomy, lymphatics

INTRODUCTION

Anatomy of the Japanese monkey has been limited to topographic and comparativestudies. Studies of lymphatic system on the Japanese monkey have not beenfound 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 and2 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 dissectionusing a stereomicroscope.

RESULTS

The lymphatic vessels originating from the upper and lower lips, the eyelids andthe face (Fig. 1) entered the submandibular lymph nodes (Fig. 2) after runningalong the anterior facial vein. The vessels from a part of the lower lip entered the

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submental lymph nodes (Figs. 1 and 2) and the efferent vessels entered thesubmandibular lymph nodes. The lymphatic vessels from the auricles entered the

parotid lymph nodes (Fig. 2). The efferent vessels from the submandibular, submentaland parotid lymph nodes ran independently and entered the superficial cervicallymph nodes (Fig. 2), which were located near the junction of the external jugularand the anterior facial veins. The superficial cervical lymph nodes were one of theterminal lymph nodes in the head and neck. Another terminal lymph node was thecranial deep cervical lymph node (Fig. 3), which received the lymphatic vesselsfrom the tongue. The efferent vessels from these two terminal lymph nodes coursedtogether to make the jugular lymphatic trunk running to the venous angle.

There were two lymphatic routes in the fore-limb. The routes arose from thesubcutaneous lymphatic network extending from back of the hand to the wrist

joint. Firstly, the lymphatic vessels from this network proceeded in the anterioraspect of the fore-arm along the antebrachial cephalic and median veins and subcu-taneous branches of nerves to the elbow joint. In the upper arm, they proceededalong the cephalic vein and became four or five streaks (Fig. 4). They entered thesuperficial axillary lymph nodes (Figs. 2, 3, and 5) near the quadrangular space ofthe shoulder joint region and finally reached the deep axillary lymph nodes (Fig.5). Secondly, some of lymphatic vessels from the lymphatic network in the handinclined toward the ulnar side in the anterior aspect of fore-arm and proceededalong the basilic vein in the upper arm. This route directly entered the deep axillarylymph nodes (Fig. 5). The deep axillary lymph nodes also received subcutaneouslymphatic vessels of the thorax (Figs. 1, 2, 4 and 5). The efferent vessel of the deepaxillary lymph nodes was the subclavian lymphatic trunk. The trunk proceededalong the lateral thoracic artery and vein in turn. After extending a communicatingvessel 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 leftjugular trunk and the thoracic duct (Fig. 3).

The ventral route of the lymphatic vessels from the diaphragm, the intercostalspace 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 partof vessels from the right and left lungs proceeded behind the both bronchi andentered the bifurcational lymph nodes at the bifurcation of the trachea (Fig. 8). Theefferent vessel of the this lymph node entered the left tracheobronchial lymphnodes. The lymphatic vessels from the left tracheobronchial lymph nodes enteredthe brachiocephalic venous angle lymph nodes via the paratracheal and pretracheallymph nodes. The lymphatic vessels of the right lung entered mainly the rightmediastinal 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, parotidlymph node; SAL, superficial axillary lymph node; SCL, superficial cervical lymphnode; SML, submandibular lymph node; SUL, submental lymph node; JLT, jugularlymphatic 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, parotidgland; sb, sternal bone; t, trachea; ul, upper lip.

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bronchomediastinal lymphatic trunk. In these subjects, the trunk was observed inall the cases on the right but none on the left (Fig. 8).

The lymphatic vessels from the stomach ran parallel with the left gastric arteryand entered the left gastric lymph nodes. This lymph node received the lymphaticvessels from the spleen via the splenic lymph nodes. The hepatic lymph nodeaccepted the lymphatic vessels originating from the liver, and received a part of thelymphatic vessels from the pancreas, duodenum, and pylorus of the stomach via the

pancreaticoduodenal lymph nodes (Fig. 9). These lymph nodes belonged to a group

Figs. 4 and 5. The superficial (Fig. 4) and deep (Fig. 5) lymphatic pathway in the foreleg.

acv, antebrachial cephalic vein; bv, basilic vein.

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 lymphnode; 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).

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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 twolymphatic 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.

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ascended along the right outer surface of the thoracic aorta and turned to the left atthe 5th or 6th thoracic vertebra. Further it ascended between the left commoncarotid and subclavian arteries to the level near the superior thoracic aperture anddrained into the vein at the angle of union of the internal jugular and subclavianveins after merging with the left jugular and subclavian lymphatic trunks (Figs. 3and 8).

The right lymphatic trunk formed a common vessel near the junction of thevenous angle from the jugular, subclavian and bronchomediastinal lymphatic trunks.0The 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 samespecies 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). Thesuperficial and deep lymphatic pathway male genital organ (Figs. 14 and

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 mesentericartery; p, penis; ra, renal artery; srg, suprarenal gland; st, scrotum; tt, testis; u, ureter; ub, urinarybladder; *, the dorsal route of the lymphatic vessel from the diaphragm(d).

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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.

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

node.

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Table 1. Comparison of lymph nodes belonging to various lymphocentra

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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)

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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 describedthat 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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