J. Anat (1991), 177, pp. 67-73 With 2 figures Printed in Great Britain
67
Topography of the major superficial lymph nodes and their efferent lymph pathways in the koala (Phascolarctos cinereus)* JONATHAN J. HANGER AND TREVOR J. HEATH Department of Anatomy, University of Queensland, St Lucia, Brisbane, Queensland,
Australia 4067
(Accepted 14 January 1991) INTRODUCTION
Although disease has long been recognised as a significant cause of mortality in koalas, virtually no information is available on their immune system and its responses to disease. The peculiar susceptibility of koalas to disease and the apparent incompetence of their immune systems, particularly in combating infections, has led some research workers to suggest that the immune response in these animals may be retarded in some way (Brown et al. 1987; Brown, 1988). Virtually no information, however, is available on the lymph nodes or vessels, or other aspects of the immune system, in koalas. Furthermore, the lymphatic system of other marsupials has only been described in any detail in the American opossums (Didelphys azarae and Didelphys marsupialis) (Zimmerman, 1940; Azzali & Di Dio, 1965), and the kangaroo (Macropus spp.) (Hopwood, 1980, 1988). The aim of this study was to describe the topographical anatomy of the major superficial lymph nodes and lymph pathways in koalas to their termination in the great veins. This was achieved by gross dissection, and by using Evans Blue dye and Microfil casts. MATERIALS AND METHODS
Twenty-six koalas, of both sexes aged between 9 months and 12 years, were used. All had either died previously or were in extremis from either disease or trauma associated with road accidents or dog attack. Those animals which were in extremis and required euthanasia on humane grounds were killed by pentobarbitone sodium overdose, given by intravenous or intracardiac injection. The decision to destroy these koalas was made by a registered veterinarian not associated with the study. Superficial lymphatics were cannulated using polyethylene tubing (Dural Plastics and Engineering, Dural, New South Wales) with an internal diameter 0 5 mm for larger lymphatics and 0-2 mm drawn out over a gentle flame for smaller lymphatics. To enable clear visualisation of lymph pathways, Evans Blue dye (1 %) or Microfil (Canton Biomedical Products, Boulder, Colorado), a synthetic rubber casting compound, was injected through the cannula from a 1 ml or 2 ml syringe under moderate manual pressure. The volume varied between 0-5 and 2 ml. Drainage areas to some of the superficial lymph nodes were investigated by injecting 0 2-1 ml of Evans Blue dye through a 26 g needle inserted under the skin or the Reprint requests to Professor T. J. Heath, Department of Anatomy, University of Queensland, St Lucia, Brisbane, Queensland, Australia 4067. *
68 J. J. HANGER AND T. J. HEATH conjunctiva. The dye was taken up into the initial lymphatics draining the injection site and was then carried in larger vessels to the primary lymph node. In carcasses which were obtained more than 2 h after death, the superficial lymphatics had collapsed and were virtually invisible. Lymph nodes from these carcasses were directly injected in situ with Evans Blue dye or Microfil using a 30 g needle. RESULTS
The major superficial lymph nodes and lymph pathways are represented diagrammatically in Figures 1 and 2. In the text, the names of lymph nodes which are readily palpable in the live koala are marked with an asterisk.
Superficial lymph nodes and lymph pathways of the head and neck Mandibular lymph centre The facial lymph node* was round and approximately 5-10 mm in diameter, and it lay near the rostral border of the facial tubercle and 10-20 mm ventral to the orbit. Of 8 koalas examined, 2 had a single facial node bilaterally, 1 had two nodes on each side, and it was absent in 5 of the koalas. When present, it was the primary node draining the conjunctiva. Efferent lymph vessels from the facial node passed either to the mandibular lymph node only, or to the rostral mandibular node and the mandibular node. The rostral mandibular lymph node* was present in all the koalas studied. It was a flattened, rounded node approximately 8-15 mm in diameter, which lay close to the lateral surface of the horizontal ramus of the mandible just rostral to, and in contact with the rostral border of the masseter muscle and deep to the platysma muscle. In koalas which lacked a facial node, lymph from the conjunctiva drained either to the rostral mandibular or to the mandibular lymph node. The main efferent vessel from the rostral mandibular node traversed the superficial face of the masseter muscle to the mandibular lymph node. In some koalas there were intermediate lymph nodes, sometimes up to four, on the superficial face of the masseter muscle between the rostral mandibular node and the mandibular node. The mandibular lymph node* was located just caudolateral to the mandibular salivary gland. It was oval or irregular in shape and lay subcutaneously on the lateral border of the lingual vein. One or more vessels left the node and became afferent lymphatics to the superficial cervical lymph nodes. In some koalas, small accessory mandibular lymph nodes were present in the subcutis over the ventral aspect of the neck. They were flattened, oval or rounded in shape and varied in size, number and position. Efferent lymphatics from these nodes passed to the mandibular lymph nodes. Parotid lymph centre The parotid lymph node lay totally or partially within the parotid salivary gland, and often in contact with the dorsal border of the mandibular lymph node. Efferent lymphatics from this node became confluent with those from the mandibular lymph node, then entered the superficial cervical lymph nodes.
Superficial cervical lymph centre Two spherical or oval superficial cervical lymph nodes lay just cranial to the termination of the common jugular and subclavian veins, and deep to the
Lymph pathways in the koala
69
Facial LN
Parotid LN
.0. 7. Mandibular LN
Rostral mandibular LN R Common jugular V I R Subclavian V
Superficial cervical LN
R Cranial vena cava
Fig. 1. Diagrammatic representation of the major superficial lymph nodes and their efferent pathways in the head and neck in koalas. The facial lymph node is absent in some koalas.
Accessory superficial inguinal LN Fig. 2. Diagrammatic representation of the major superficial lymph nodes and their efferent pathways in koalas. The accessory mandibular lymph nodes, which are present in some koalas, are not shown. Ventrodorsal view.
omotransversarius muscle. Efferent lymph vessels from the mandibular and parotid lymph nodes entered the more rostral of the two nodes, and vessels leaving this node then entered the more caudal of the two nodes. Efferent lymph vessels from this caudal node coalesced almost immediately to form a single large vessel, containing numerous valves, which entered the bloodstream at the confluence of the common jugular and the subclavian veins.
70
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Superficial lymph nodes and lymph pathways of the trunk Superficial inguinal lymph centre The superficial inguinal lymph node was generally the largest node in koalas, measuring 10-20 mm in length in the adult. It was usually flattened and oval in shape, and its position was variable. In females it was usually deep in the groove between the medial muscles of the thigh, and most commonly just cranial to the pectineus muscle. In females with pouch young, the nodes were covered by the lateral outpocketings of the pouch. In males, the superficial inguinal node lay more medially, close to the origin of the epipubic bones, and was sometimes medial to the epipubic bone near the base of the scrotum. Although commonly the superficial inguinal lymph node was a single discrete node, some koalas had one or more accessory superficial inguinal nodes. These accessory nodes were oval or rounded in shape, and 5-10 mm long. Some lay between the left and right superficial inguinal nodes and interrupted lymphatic connections between the two, whereas others had lymphatic connections with only one of the principal nodes. Afferent lymph vessels entered over much of that surface of the node which faced away from the abdominal wall. Efferent lymphatics emerged from the deep face of the node, which was flattened. They coalesced on the surface of the node to form the inguinoaxillary trunk. In most koalas this was the only efferent lymph pathway from the superficial inguinal lymph node. Three koalas had anomalous efferent pathways: in 2 of them some efferent vessels from the superficial inguinal node passed through the femoral canal to the medial iliac lymph nodes; and in another the inguinoaxillary trunk was absent on the left side, and all efferent lymphatics from the left node crossed to the right superficial inguinal node.
Inguinoaxillary trunk This was the longest lymph vessel in koalas, and conveyed lymph from the superficial inguinal lymph node to the deep axillary lymph node. It was approximately 4 mm across, with bicuspid valves at intervals of 5-10 mm along its length. It followed a virtually straight path from the cranial pole of the superficial inguinal node over the apex of the epipubic bone to the axilla. In its course along the ventrolateral aspect of the abdomen and thorax it passed between the cutaneous trunci and the musculature of the abdomen and thorax. Its terminal portion passed between the fibres of the superficial pectoral muscle, before dividing into three to five branches which entered the deep axillary lymph nodes. In many koalas there was some bifurcation of the trunk, but there were seldom more than two branches at any one position, and these ran parallel and closely applied to one another. Axillary lymph centre There were two groups of lymph nodes in this lymph centre: the superficial axillary lymph node and the deep axillary lymph nodes. The superficial axillary lymph node* was elongated and oval shaped, and lay in the fascia between the proximal portion of the biceps muscle and the body of the superficial pectoral muscle, protruding beyond the caudolateral border of this muscle. In the adult koala it was 12-20 mm long and 6-8 mm wide. In one koala there were two superficial axillary lymph nodes on both sides, but in all the others this node was single. One to three small efferent lymph vessels left the superficial axillary node and entered the most caudal of the deep axillary nodes.
Lymph pathways in the koala
71
The deep axillary lymph node in some koalas was a single large node, but more commonly there were two to four smaller nodes in a row. When single the node was an elongated oval shape, about 20 x 9 mm in the adult, and lay against the lateral aspect of the thoracic wall between the second and fourth ribs. In koalas with more than one deep axillary node, they were smaller and more rounded, and lay in a line between the first intercostal space and the fourth rib. The most caudal node was usually the largest, and received most of the efferent lymph vessels from the superficial axillary node. The main afferent vessel to the deep axillary nodes was the inguinoaxillary trunk, which delivered lymph directly from the superficial inguinal lymph node. Before entering the axillary region this trunk divided into three to five branches, which entered the one or two most caudal of the nodes. Smaller vessels also entered these nodes from the superficial axillary node and directly from adjacent tissues. In koalas with a single deep axillary node its efferent lymph vessel was approximately 3 mm in diameter, and it had numerous valves along its length. This delivered lymph from the cranial pole of the node to the bloodstream near the confluence of the common jugular and subclavian veins, just medial to the level of the first rib. If two or more deep axillary nodes were present, they were connected by a variable number of lymph vessels. Efferent lymph left the most cranial of these nodes through a single large vessel, and entered the bloodstream as described above. DISCUSSION
The overall topography of the lymphatic system of the koala resembles that of the American opossums (Azzali & Di Dio, 1965) and the kangaroo (Hopwood, 1980, 1988), but differences occur in the location and even the presence of some lymph nodes, and in the number of nodes in different lymph centres. A major difference in the superficial lymphatic system, however, exists between these marsupials and eutherian mammals in that the marsupials have a large inguinoaxillary trunk on either side of the ventral midline. This trunk has been variously referred to in opossums as the 'thoraco-epigastric collecting trunks' (Wood, 1924), 'lateral lymph trunks' (Zimmerman, 1940; Kampmeier, 1969) and 'subcutaneous abdomino-thoracic efferent collecting vessel' (Azzali & Di Dio, 1965), and in the kangaroo as the 'inguino-axillary trunk' (Hopwood, 1980). The latter term has been used in this paper as it most accurately describes the position and course of the trunk. This trunk delivers lymph from the superficial inguinal lymph node to another lymph node - the deep axillary node. This is in contrast to the situation in eutherian mammals, in which the large lymphatic ducts drain directly into the bloodstream (Yoffey & Courtice, 1970; Schummer et al. 1981). In most koalas the inguinoaxillary trunk is the only route of efferent lymph from the superficial inguinal node, and consequently the deep axillary lymph node receives all the lymph from this node. This also contrasts with the situation in domestic animals and other eutherian mammals, in which efferent lymph vessels from the superficial inguinal node pass through the inguinal canal to the medial iliac or iliofemoral lymph nodes, and reach the bloodstream through the thoracic duct (Kampmeier, 1969; Yoffey & Courtice, 1970; Evans & Christensen, 1979; Schummer et al. 1981; Heath & Kerlin, 1986). The drainage pathway provided by the inguinoaxillary trunk may be particularly important in the koala, which spends a large percentage of its time - up to 80 % inactive and in an upright position (Smith, 1979). The pressure of the adjacent tree on
72
J. J. HANGER AND T. J. HEATH
the lymphatic trunk, coupled with the effects of the numerous valves, and intrinsic contractility of this vessel, must all be important in facilitating the return of lymph against the force of gravity. Another notable feature of the superficial lymphatic system of koalas is the absence of popliteal and subiliac lymph nodes, which are present in most of the domestic species (Schummer et al. 1981). The drainage areas of these lymph nodes in domestic animals are most likely encompassed by those of the relatively large superficial inguinal and axillary lymph nodes in koalas. Most of the superficial lymph nodes in koalas are readily accessible for palpation or biopsy during clinical examination of the koala patient. The facial lymph node, which lies rostral to the facial tubercle, is variably present and is relatively small in size when normal. Nevertheless, this node should be readily palpable if enlarged due to inflammation or neoplasia. The rostral mandibular lymph node, which has not been described in any other marsupial or domestic species, lies just rostral to the masseter muscle and is easily located and palpated even when normal in size. Similarly, the superficial inguinal lymph node, although variable in position, is easily located and readily palpable. The mandibular lymph node may be difficult to locate when normal in size due to its close association with the mandibular salivary gland, but is readily identified and palpable when affected by inflammatory or neoplastic enlargement. The superficial axillary lymph node may be difficult to locate in the live animal due to its position in the axilla, but once located can be readily palpated. SUMMARY
The koala has an inguinoaxillary lymph trunk on either side of the ventral midline, and this carries efferent lymph from the superficial inguinal lymph node directly to the deep axillary lymph node. The superficial lymph nodes are large and soft compared with those of the domestic species, and each lymph centre usually contains only one or two large lymph nodes. Koalas have a rostral mandibular lymph node which has not been described in other species, but lack popliteal and subiliac lymph nodes. The superficial lymph nodes which are readily palpable in the live koala are the facial, rostral mandibular, mandibular, superficial axillary and superficial inguinal. All superficial lymph pathways terminate at the confluence of the common jugular and subclavian veins. We acknowledge with thanks the help of Mr Don Burnett of the Koala Preservation Society of Queensland, and World Koala Research Inc. REFERENCES
AZZALI, G. & Di Dio, L. J. A. (1965). The lymphatic system of Didelphys azarae and Didelphys marsupialis. American Journal of Anatomy 116, 449-470. BROWN, A. S. (1988). The health of Australia's koalas: more research is needed urgently. Medical Journal of Australia 149, 662-664. BROWN, A. S., GIRJEs, A. A., LAVIN, M. F., TIMMs, P. & WOOLCOCK, J. B. (1987). Chlamydial disease in koalas. Australian Veterinary Journal 64, 346-350. EVANS, H. E. & CHRISTENSEN, G. C. (1979). Miller's Anatomy of the Dog. Philadelphia: W. B. Saunders. HEATH, T. J. & KERLIN, R. J. (1986). Lymph drainage from the mammary gland in sheep. Journal of Anatomy 144, 61-70. HOPWOOD, P. R. (1980). The Lymphatic System of Kangaroos with Special Reference to Meat Inspection of the Kangaroo Carcass. Monograph, University of Sydney.
Lymph pathways in the koala
73
HOPWOOD, P. R. (1988). An investigation of the topography of the lymphatic system of the grey kangaroo (Macropus giganteus). I. The superficial lymphatic system. Journal of Anatomy 157, 181-195. KAMPMEIER, 0. F. (1969). Evolution and Comparative Morphology of the Lymphatic System. Springfield, Illinois: Thomas. SCHUMMER, A., WILKENS, H., VOLLMERHAUS, B. & HABERMEHL, K. (1981). The Anatomy of the Domestic Animals, Vol. 3. Berlin, Hamburg: Verlag Paul Parey. SMITH, M. (1979). Behaviour of the koala, Phascolarctos cinereus Goldfuss, in captivity. I. Non-social behaviour. Australian Wildlife Research 6, 117-129. WOOD, G. N. (1924). The lymphatics of the opossum. Anatomical Record 27, 192-193. YOFFEY, J. M. & COURTICE, F. C. (1970). Lymphatics, Lymph and the Lymphomyeloid Complex. London and New York: Academic Press. ZIMMERMAN, A. A. (1940). Origin and Development of the Lymphatic System in the Opossum. Illinois Medical and Dental Monographs, Vol. in, nos. 1-2. Urbana, Illinois: University of Illinois Press (cited by Hopwood, 1980).
67
Topography of the major superficial lymph nodes and their efferent lymph pathways in the koala (Phascolarctos cinereus)* JONATHAN J. HANGER AND TREVOR J. HEATH Department of Anatomy, University of Queensland, St Lucia, Brisbane, Queensland,
Australia 4067
(Accepted 14 January 1991) INTRODUCTION
Although disease has long been recognised as a significant cause of mortality in koalas, virtually no information is available on their immune system and its responses to disease. The peculiar susceptibility of koalas to disease and the apparent incompetence of their immune systems, particularly in combating infections, has led some research workers to suggest that the immune response in these animals may be retarded in some way (Brown et al. 1987; Brown, 1988). Virtually no information, however, is available on the lymph nodes or vessels, or other aspects of the immune system, in koalas. Furthermore, the lymphatic system of other marsupials has only been described in any detail in the American opossums (Didelphys azarae and Didelphys marsupialis) (Zimmerman, 1940; Azzali & Di Dio, 1965), and the kangaroo (Macropus spp.) (Hopwood, 1980, 1988). The aim of this study was to describe the topographical anatomy of the major superficial lymph nodes and lymph pathways in koalas to their termination in the great veins. This was achieved by gross dissection, and by using Evans Blue dye and Microfil casts. MATERIALS AND METHODS
Twenty-six koalas, of both sexes aged between 9 months and 12 years, were used. All had either died previously or were in extremis from either disease or trauma associated with road accidents or dog attack. Those animals which were in extremis and required euthanasia on humane grounds were killed by pentobarbitone sodium overdose, given by intravenous or intracardiac injection. The decision to destroy these koalas was made by a registered veterinarian not associated with the study. Superficial lymphatics were cannulated using polyethylene tubing (Dural Plastics and Engineering, Dural, New South Wales) with an internal diameter 0 5 mm for larger lymphatics and 0-2 mm drawn out over a gentle flame for smaller lymphatics. To enable clear visualisation of lymph pathways, Evans Blue dye (1 %) or Microfil (Canton Biomedical Products, Boulder, Colorado), a synthetic rubber casting compound, was injected through the cannula from a 1 ml or 2 ml syringe under moderate manual pressure. The volume varied between 0-5 and 2 ml. Drainage areas to some of the superficial lymph nodes were investigated by injecting 0 2-1 ml of Evans Blue dye through a 26 g needle inserted under the skin or the Reprint requests to Professor T. J. Heath, Department of Anatomy, University of Queensland, St Lucia, Brisbane, Queensland, Australia 4067. *
68 J. J. HANGER AND T. J. HEATH conjunctiva. The dye was taken up into the initial lymphatics draining the injection site and was then carried in larger vessels to the primary lymph node. In carcasses which were obtained more than 2 h after death, the superficial lymphatics had collapsed and were virtually invisible. Lymph nodes from these carcasses were directly injected in situ with Evans Blue dye or Microfil using a 30 g needle. RESULTS
The major superficial lymph nodes and lymph pathways are represented diagrammatically in Figures 1 and 2. In the text, the names of lymph nodes which are readily palpable in the live koala are marked with an asterisk.
Superficial lymph nodes and lymph pathways of the head and neck Mandibular lymph centre The facial lymph node* was round and approximately 5-10 mm in diameter, and it lay near the rostral border of the facial tubercle and 10-20 mm ventral to the orbit. Of 8 koalas examined, 2 had a single facial node bilaterally, 1 had two nodes on each side, and it was absent in 5 of the koalas. When present, it was the primary node draining the conjunctiva. Efferent lymph vessels from the facial node passed either to the mandibular lymph node only, or to the rostral mandibular node and the mandibular node. The rostral mandibular lymph node* was present in all the koalas studied. It was a flattened, rounded node approximately 8-15 mm in diameter, which lay close to the lateral surface of the horizontal ramus of the mandible just rostral to, and in contact with the rostral border of the masseter muscle and deep to the platysma muscle. In koalas which lacked a facial node, lymph from the conjunctiva drained either to the rostral mandibular or to the mandibular lymph node. The main efferent vessel from the rostral mandibular node traversed the superficial face of the masseter muscle to the mandibular lymph node. In some koalas there were intermediate lymph nodes, sometimes up to four, on the superficial face of the masseter muscle between the rostral mandibular node and the mandibular node. The mandibular lymph node* was located just caudolateral to the mandibular salivary gland. It was oval or irregular in shape and lay subcutaneously on the lateral border of the lingual vein. One or more vessels left the node and became afferent lymphatics to the superficial cervical lymph nodes. In some koalas, small accessory mandibular lymph nodes were present in the subcutis over the ventral aspect of the neck. They were flattened, oval or rounded in shape and varied in size, number and position. Efferent lymphatics from these nodes passed to the mandibular lymph nodes. Parotid lymph centre The parotid lymph node lay totally or partially within the parotid salivary gland, and often in contact with the dorsal border of the mandibular lymph node. Efferent lymphatics from this node became confluent with those from the mandibular lymph node, then entered the superficial cervical lymph nodes.
Superficial cervical lymph centre Two spherical or oval superficial cervical lymph nodes lay just cranial to the termination of the common jugular and subclavian veins, and deep to the
Lymph pathways in the koala
69
Facial LN
Parotid LN
.0. 7. Mandibular LN
Rostral mandibular LN R Common jugular V I R Subclavian V
Superficial cervical LN
R Cranial vena cava
Fig. 1. Diagrammatic representation of the major superficial lymph nodes and their efferent pathways in the head and neck in koalas. The facial lymph node is absent in some koalas.
Accessory superficial inguinal LN Fig. 2. Diagrammatic representation of the major superficial lymph nodes and their efferent pathways in koalas. The accessory mandibular lymph nodes, which are present in some koalas, are not shown. Ventrodorsal view.
omotransversarius muscle. Efferent lymph vessels from the mandibular and parotid lymph nodes entered the more rostral of the two nodes, and vessels leaving this node then entered the more caudal of the two nodes. Efferent lymph vessels from this caudal node coalesced almost immediately to form a single large vessel, containing numerous valves, which entered the bloodstream at the confluence of the common jugular and the subclavian veins.
70
J. J. HANGER AND T. J. HEATH
Superficial lymph nodes and lymph pathways of the trunk Superficial inguinal lymph centre The superficial inguinal lymph node was generally the largest node in koalas, measuring 10-20 mm in length in the adult. It was usually flattened and oval in shape, and its position was variable. In females it was usually deep in the groove between the medial muscles of the thigh, and most commonly just cranial to the pectineus muscle. In females with pouch young, the nodes were covered by the lateral outpocketings of the pouch. In males, the superficial inguinal node lay more medially, close to the origin of the epipubic bones, and was sometimes medial to the epipubic bone near the base of the scrotum. Although commonly the superficial inguinal lymph node was a single discrete node, some koalas had one or more accessory superficial inguinal nodes. These accessory nodes were oval or rounded in shape, and 5-10 mm long. Some lay between the left and right superficial inguinal nodes and interrupted lymphatic connections between the two, whereas others had lymphatic connections with only one of the principal nodes. Afferent lymph vessels entered over much of that surface of the node which faced away from the abdominal wall. Efferent lymphatics emerged from the deep face of the node, which was flattened. They coalesced on the surface of the node to form the inguinoaxillary trunk. In most koalas this was the only efferent lymph pathway from the superficial inguinal lymph node. Three koalas had anomalous efferent pathways: in 2 of them some efferent vessels from the superficial inguinal node passed through the femoral canal to the medial iliac lymph nodes; and in another the inguinoaxillary trunk was absent on the left side, and all efferent lymphatics from the left node crossed to the right superficial inguinal node.
Inguinoaxillary trunk This was the longest lymph vessel in koalas, and conveyed lymph from the superficial inguinal lymph node to the deep axillary lymph node. It was approximately 4 mm across, with bicuspid valves at intervals of 5-10 mm along its length. It followed a virtually straight path from the cranial pole of the superficial inguinal node over the apex of the epipubic bone to the axilla. In its course along the ventrolateral aspect of the abdomen and thorax it passed between the cutaneous trunci and the musculature of the abdomen and thorax. Its terminal portion passed between the fibres of the superficial pectoral muscle, before dividing into three to five branches which entered the deep axillary lymph nodes. In many koalas there was some bifurcation of the trunk, but there were seldom more than two branches at any one position, and these ran parallel and closely applied to one another. Axillary lymph centre There were two groups of lymph nodes in this lymph centre: the superficial axillary lymph node and the deep axillary lymph nodes. The superficial axillary lymph node* was elongated and oval shaped, and lay in the fascia between the proximal portion of the biceps muscle and the body of the superficial pectoral muscle, protruding beyond the caudolateral border of this muscle. In the adult koala it was 12-20 mm long and 6-8 mm wide. In one koala there were two superficial axillary lymph nodes on both sides, but in all the others this node was single. One to three small efferent lymph vessels left the superficial axillary node and entered the most caudal of the deep axillary nodes.
Lymph pathways in the koala
71
The deep axillary lymph node in some koalas was a single large node, but more commonly there were two to four smaller nodes in a row. When single the node was an elongated oval shape, about 20 x 9 mm in the adult, and lay against the lateral aspect of the thoracic wall between the second and fourth ribs. In koalas with more than one deep axillary node, they were smaller and more rounded, and lay in a line between the first intercostal space and the fourth rib. The most caudal node was usually the largest, and received most of the efferent lymph vessels from the superficial axillary node. The main afferent vessel to the deep axillary nodes was the inguinoaxillary trunk, which delivered lymph directly from the superficial inguinal lymph node. Before entering the axillary region this trunk divided into three to five branches, which entered the one or two most caudal of the nodes. Smaller vessels also entered these nodes from the superficial axillary node and directly from adjacent tissues. In koalas with a single deep axillary node its efferent lymph vessel was approximately 3 mm in diameter, and it had numerous valves along its length. This delivered lymph from the cranial pole of the node to the bloodstream near the confluence of the common jugular and subclavian veins, just medial to the level of the first rib. If two or more deep axillary nodes were present, they were connected by a variable number of lymph vessels. Efferent lymph left the most cranial of these nodes through a single large vessel, and entered the bloodstream as described above. DISCUSSION
The overall topography of the lymphatic system of the koala resembles that of the American opossums (Azzali & Di Dio, 1965) and the kangaroo (Hopwood, 1980, 1988), but differences occur in the location and even the presence of some lymph nodes, and in the number of nodes in different lymph centres. A major difference in the superficial lymphatic system, however, exists between these marsupials and eutherian mammals in that the marsupials have a large inguinoaxillary trunk on either side of the ventral midline. This trunk has been variously referred to in opossums as the 'thoraco-epigastric collecting trunks' (Wood, 1924), 'lateral lymph trunks' (Zimmerman, 1940; Kampmeier, 1969) and 'subcutaneous abdomino-thoracic efferent collecting vessel' (Azzali & Di Dio, 1965), and in the kangaroo as the 'inguino-axillary trunk' (Hopwood, 1980). The latter term has been used in this paper as it most accurately describes the position and course of the trunk. This trunk delivers lymph from the superficial inguinal lymph node to another lymph node - the deep axillary node. This is in contrast to the situation in eutherian mammals, in which the large lymphatic ducts drain directly into the bloodstream (Yoffey & Courtice, 1970; Schummer et al. 1981). In most koalas the inguinoaxillary trunk is the only route of efferent lymph from the superficial inguinal node, and consequently the deep axillary lymph node receives all the lymph from this node. This also contrasts with the situation in domestic animals and other eutherian mammals, in which efferent lymph vessels from the superficial inguinal node pass through the inguinal canal to the medial iliac or iliofemoral lymph nodes, and reach the bloodstream through the thoracic duct (Kampmeier, 1969; Yoffey & Courtice, 1970; Evans & Christensen, 1979; Schummer et al. 1981; Heath & Kerlin, 1986). The drainage pathway provided by the inguinoaxillary trunk may be particularly important in the koala, which spends a large percentage of its time - up to 80 % inactive and in an upright position (Smith, 1979). The pressure of the adjacent tree on
72
J. J. HANGER AND T. J. HEATH
the lymphatic trunk, coupled with the effects of the numerous valves, and intrinsic contractility of this vessel, must all be important in facilitating the return of lymph against the force of gravity. Another notable feature of the superficial lymphatic system of koalas is the absence of popliteal and subiliac lymph nodes, which are present in most of the domestic species (Schummer et al. 1981). The drainage areas of these lymph nodes in domestic animals are most likely encompassed by those of the relatively large superficial inguinal and axillary lymph nodes in koalas. Most of the superficial lymph nodes in koalas are readily accessible for palpation or biopsy during clinical examination of the koala patient. The facial lymph node, which lies rostral to the facial tubercle, is variably present and is relatively small in size when normal. Nevertheless, this node should be readily palpable if enlarged due to inflammation or neoplasia. The rostral mandibular lymph node, which has not been described in any other marsupial or domestic species, lies just rostral to the masseter muscle and is easily located and palpated even when normal in size. Similarly, the superficial inguinal lymph node, although variable in position, is easily located and readily palpable. The mandibular lymph node may be difficult to locate when normal in size due to its close association with the mandibular salivary gland, but is readily identified and palpable when affected by inflammatory or neoplastic enlargement. The superficial axillary lymph node may be difficult to locate in the live animal due to its position in the axilla, but once located can be readily palpated. SUMMARY
The koala has an inguinoaxillary lymph trunk on either side of the ventral midline, and this carries efferent lymph from the superficial inguinal lymph node directly to the deep axillary lymph node. The superficial lymph nodes are large and soft compared with those of the domestic species, and each lymph centre usually contains only one or two large lymph nodes. Koalas have a rostral mandibular lymph node which has not been described in other species, but lack popliteal and subiliac lymph nodes. The superficial lymph nodes which are readily palpable in the live koala are the facial, rostral mandibular, mandibular, superficial axillary and superficial inguinal. All superficial lymph pathways terminate at the confluence of the common jugular and subclavian veins. We acknowledge with thanks the help of Mr Don Burnett of the Koala Preservation Society of Queensland, and World Koala Research Inc. REFERENCES
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