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Patterns of Lymphatic Drainage in the Adultlaboratory J. Anat. (1971), 109, 3, pp. 369-383 369 With 11 figures Printed in Great Britain Patterns of lymphatic drainage in the adult laboratory rat NICHOLAS L. TILNEY Department of Surgery, Peter Bent Brigham Hospital, and Harvard Medical School, Boston, Massachusetts (Accepted 27 April 1971) INTRODUCTION This study was undertaken to define and elucidate patterns of lymphatic drainage in the adult laboratory rat. The incentive for the work arose from investigations into the role of regional lymphatics in the sensitization of the host by skin allografts. It has become clear that the response of rats to antigens, investigated increasingly in the available inbred strains, requires an accurate knowledge of lymphoid anatomy and lymphatic drainage routes. Examinations of the lymphatics of specific body areas of the rat have appeared sporadically in the literature, but descriptions of regional drainage patterns, especially of peripheral sites, are unavailable. Previous investigations by Job (1919), Greene (1935) and Sanders & Florey (1940) have con- centrated primarily upon the location of the lymphoid tissues. Miotti (1965) has stressed visceral drainage, and Higgins (1925) has described the lymphatic system of the newborn rat. A more complete definition of both somatic and visceral lymphatic routes is presented. MATERIALS AND METHODS One hundred and thirty normal adult rats of both sexes, each weighing between 150 and 300 g, were studied. The animals came from five strains: each inbred - Oxford strains of the albino (AO), hooded (HO), agouti (DA), and F1 hybrid of the HO and DA strains - and 'stock' animals from a closed outbred albino colony. Under ether anaesthesia, the site for cutaneous injection was clipped or a serous cavity entered for visceral injection. The majority of animals were killed by ether overdose and dissected within a few minutes because of the rapidity of uptake of the injected material by lymphoid tissue. Several rats were studied between 48 h and 6 weeks after injection to elucidate possible variations in the distribution of the dye with time. Regional nodes and all secondary drainage sites were examined. Three types of injected material were employed. The location of lymph nodes was demonstrated by the intraperitoneal injection of pontamine sky blue, 10-14 days before dissection. This was administered as a sterile 5 00 solution in distilled water at a dose of 1 ml per 100 g body weight. Macrophages coloured with dye remained in lymph nodes long after surrounding tissues have cleared and allowed the identification of even minute lymphoid aggregations. The cutaneous areas were mapped by intra- dermal injections of 0-05-0d10 ml of colloidal carbon (Pelikan Ink, Guinther Wagner, Germany). This material filled lymphatic channels and readily stained draining lymph nodes. Similar injections of 1311 human serum albumin (Radiochemical Centre, 24 ANA 109 370 NICHOLAS L. TILNEY Amersham, Bucks, England) were used to confirm these patterns of drainage. The regional lymph nodes were removed and their radioactive uptake measured in a gamma scintillation spectrometer (Packard Series 410A). Passive muscular motion was helpful in forcing the dye along peripheral lymph- atics. Subserosal injections of hollow viscera or subcapsular injections of solid organs using a no. 30 needle satisfactorily demonstrated visceral lymphatic patterns. The lymph trunks between lymph node groups were visualized by injections of minute volumes of India ink directly into the nodal substance: gentle external pressure on the node caused filling of the efferent lymphatics. Accurate localization of 'lymphatic taps' - the valved junctions of the major lymph ducts with the subclavian veins - was facilitated by total replacement of the circulating blood volume of the animal with saline. Carbon particles could then easily be seen flowing from the lymph ducts into the veins. Lymph node groups have been classified into somatic nodes, which drain the skin and underlying musculature (Table 1), and visceral nodes, which drain primarily the thoracic, abdominal and pelvic organs (Table 2). Somatic nodes generally lie external to skeletal muscle in subcutaneous or areolar tissue, or in fossae between muscle masses. These nodes have been divided functionally into a peripheral and central group. The peripheral group of somatic nodes drains skin and musculo-skeletal sites only. The central group drains similar anatomical areas, but also receives lymphatic channels from peripheral nodes. The nomenclature of the lymph nodes is that of Job (1915) and Sanders & Florey (1940), although modifications have been made to emphasize specific drainage patterns (Fig. 1). 'Lymph trunks' were defined as the large channels connecting various groups of nodes. 'Lymphatic ducts' drain particular groups of nodes and empty directly into the cisterna chyli, or into the subclavian veins through the 'lymphatic taps'. RESULTS The location of lymphoid tissue and distribution of lymphatic channels was con- sistent in individual animals and among the strains of rats used in the study, despite occasional variation in size and number of nodes. Well-defined cutaneous areas were drained by specific groups of nodes (Fig. 2). Nodes within these groups drained distinct sites, although there was usually some overlap between adjacent nodes. Extensive lymphatic plexuses, present throughout the subdermis and in the sub- mucosa of hollow viscera, emptied into constant lymph channels which generally followed veins toward the regional nodes. No peripheral channels entered any body cavity with perforating blood vessels. Junctions between lymphatics and veins other than at the subclavian veins, or direct lymphatico-venous anastomoses within lymph nodes themselves, were not demonstrated. Somatic nodes Head and neck The peripheral lymph nodes draining the head and neck are the superficial cervical, facial and internal jugular groups (Fig. 3). The superficial cervical nodes lie at the upper poles of the submandibular glands and drain the tongue and nasolabial Patterns of lymphatic drainage in the adult laboratory rat 371 lymphatic plexus through channels running between the borders of the digastric and masseter muscles. A small efferent lymphatic curls around the lateral aspect of each submandibular gland to join efferent channels from the facial nodes, or to enter this group directly. Fig. 1. Lymph node groups in the dissected adult rat. Nodes lying dorsally are demonstrated by reflecting muscles and viscera. Adapted from Sanders & Florey (1940). The facial nodes lie dorsal to the lower poles of the submandibular glands at the junction of the anterior and posterior facial veins with the external jugular veins. They drain the skin of the head and the ventral aspect and sides of the neck through lymph vessels running with the corresponding facial veins. A large efferent facial trunk loops laterally around each sternocleidomastoid muscle to enter the posterior cervical nodes. As has been noted by Higgins (1925) in studies of newborn rats, a small area of the forehead has minimal lymphatic drainage and presumably repre- 24-2 372 NICHOLAS L. TILNEY sents a lymphatic watershed. Rarely, a tiny posterior auricular lymph node drains the ear, although generally lymphatics with the auricular vein empty into the posterior facial channel. /Cz Cervical lymph nodes E] Inguinal \9 5 Brachial m Popliteal = Axillary Gluteal Fig. 2. The cutaneous areas drained by somatic lymph node groups. Table 1. Somatic lymph nodes of the rat Region Lymph and type node group Location Area drained Efferent drainage Head and neck Peripheral Superficial cervical Upper pole of sub- Nasolabial plexus Central cervical nodes nodes mandibular gland Facial Junction of facial Head and neck Central cervical nodes veins Internal jugular Ventral to brachial Deep cervical Central cervical nodes plexus viscera Central Posterior cervical Dorsal to brachial Peripheral cervical Cervical duct nodes plexus nodes, deep cervical viscera Upper extremity, Trunk Peripheral Brachial Triceps muscle Upper extremities, Axillary nodes nodes shoulders, chest Central Axillary Axilla Upper extrem- Subclavian duct nodes ities, trunk, brachial nodes Hindquarters, Lower extremit y Peripheral Inguinal Flank Thigh, haunches, Axillary nodes nodes scrotum, lateral tail Popliteal Popliteal space Foot, hind leg Lumbar, inguinal nodes Tail Gluteal Sciatic foramen Tail Caudal, lumbar, inguinal, popliteal nodes Patterns of lymphatic drainage in the adult laboratory rat 373 The internal jugular nodes lie close to the posterior cervical nodes, but belong functionally to the peripheral group. They are ventral to each brachial plexus, immediately lateral to the carotid sheath, and drain the pharynx, larynx and the proximal part of the oesophagus through pharyngeal lymphatics running along the surface of the deep cervical muscles. A short lymphatic from each internal jugular node enters the adjacent posterior cervical node directly. The posterior cervical nodes lie dorsal to the brachial plexus on each side. These single central nodes drain all peripheral nodes in the neck and may receive minor tributaries from deep cervical structures. They empty into the posterior aspect of each subclavian vein through large cervical lymph ducts which run into the thorax dorsal to the carotid sheaths. Anterior facial lymphatic M ms. Nasolabial lymphatic Masseter ma. Superficial cervical nodesDiatcm. Parotid gland Submandibular gland Posterior facial lymphatic Internal jugular node IS I( - ~~~~~Pharyngeal
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