The Lymphatic Pathways from the Peritoneal Cavity: a Lymphangiographic Study in the Rat
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The Lymphatic Pathways from the Peritoneal Cavity: A Lymphangiographic Study in the Rat TORD OLIN AND TOM SALDEEN (Institute of Pathology, the Roentgendiagnostic Department@sand the Institute of Phy8iology, University of Lund, Lund, Sweden) SUMMARY The lymphatic drainage from the peritoneal cavity was studied radiographically following intraperitoneal injection of Thorotrast. The lymphatics of the diaphragm were filled first, draining both cranially and caudally. The most important pathways from the peritoneal cavity were the parasternal lymphatics. Only a small amount of Thorotrast was found in the lymph of the thoracic duct. Tumors in the peritoneal cavity often spread via the in the rat but did not go into detail concerning the lym lymphatics. A thorough knowledge of the lymphatic phatic drainage of the peritoneal cavity. As far as pos pathways from the peritoneal cavity is therefore of im sible his terminology has been used. portance. In studies of the absorption from the perito neal cavity into the lymphatics, different tracer substances MATERIALS AND METHODS have been used, such as erythrocytes (8, 12), small parti Sixty Sprague-Dawley rats weighing 150—200gm. were des (5, 12, 13, 18), colored substances (10), and roentgen used. Five ml. of 20 per cent Thorotrast (Testagar & Co., contrast media (2—4,7, 16, 22, 24, 25). The lymphatics USA) were injected intraperitoneally, and the rats were of the diaphragm have been shown to be the only route sacrificed and radiographed 10 hours later by a 4-valve for this drainage in man (4), and in many other species roentgen-apparatus (Scandia Optimatic, Elema, Sweden). such as dog (4, 5, 7, 18), cat (9), rabbit (2—4, 6, 13, 16, This interval seemed to be optimal—2 hours was often 25), rat (2, 3, 10, 22), and mouse (24). too short a period. Film focus distance was 1 m. and The rat is one of the most frequently used animaLs for the focal spot, 0.6 X 0.6 mm. No intensifying screens or tumor experiments. The lymphatic pathways from the grids were used. The film, Microcard (Gaevert), was peritoneal cavity have been previously examined in the exposed with 1000 mAs and 70—80kv. The rats were rat by means of lymphangiography by Menville and Ané radiographed in three different positions: lateral, antero (22). They injected 0.5 ml. Thorotrast intraperitoneally posterior, and oblique. Before the exposure the perito into three rats and radiographed the animals at 24 hours neal cavity was rinsed, clearing away residual Thorotrast and again 2 weeks later. A right and a left lymphatic solution. In some cases the liver and spleen were re duct were demonstrated in the chest, but their exact moved. To estimate the lowest concentration at which localizations were not described, probably because the an average-sized lymphatic would be visible in radio animals were examined in only one position. graphs, polyethylene tubes (PE 10, 0.28 mm.) were filled Bennet and Shivas (3) injected 1 ml. Angiopac (an with Thorotrast solutions of different concentrations. aqueous emulsion of ethyl iodostearate, Union Chimique These tubes were placed in a rat and radiographed. The Belge) intraperitoneally into ten rats. Each day one rat lowest concentration at which a tube could be identified was sacrificed and radiographed. On lateral chest films a on the radiograms was about 1.2 per cent. large lymph trunk was seen behind the upper part of the In seven animals the thoracic duct was catheterized in sternum. Furthermore, some mediastinal lymph nodes the neck with a polyethylene tube, PE 10, according to a were opacified. method described by Saldeen and Linder (28). This Barer (2) injected 2—4cc. of radiopaque materials catheterization was performed prior to the intraperitoneal (Thorotrast, Angiopac, Micropaque, Pyelosil, or Uro injection. The lymph from the duct was sampled at 1, grafin) into fifteen rats. The substances rapidly entered 2, and 10 hours following the injection. The concentra the diaphragmatic lymphatics and passed up by an an tion of Thorotrast in the lymph was analyzed in a scintilla tenor route through the thorax to the anterior mediastinal tion-counter with a well-crystal, in the energy ranges from glands. 50 to 400 keV. A 20 per cent Thorotrast solution was More detailed information was desired, however, and used as a standard. Following the 10-hour sampling this investigation was therefore performed. the animals were sacrificed. Thorotrast (0.05 ml.) was Job (17) described the anatomy of the lymphatic system injected into the thoracic duct in a retrograde direction, Received for publication April 13, 1964. and the animals were radiographed. 1700 Downloaded from cancerres.aacrjournals.org on September 30, 2021. © 1964 American Association for Cancer Research. OLIN AND SALDEEN—LymphatiC Pathways from Peritoneal Cavity 1701 The dead animals were autopsied, and organs of special ever, from the intestine, not from the diaphragm. Some interest—i.e., lymph nodes, liver, spleen, kidneys, and rats were placed on a dry diet prior to the experiment to adrenals—were studied microscopically. The sections diminish the flow of chyle, but even then the duct was not were stained with haematoxylin-eosin and Best's carmin visible on the radiograms. In the seven rats in which the (13). thoracic duct was catheterized, the amount of lymph col lected the 1st hour following the intraperitoneal injection RESULTS had a mean volume of 3.1 ml. During the 2d hour 3.0 ml. After the intraperitoneal injection of Thorotrast, the lymph drained, and during the following 8 hours 11.0 ml. lymphatics of the diaphragm were generally visualized in lymph was collected. The concentration of Thorotrast all animals by the end of 1 hour. The lymphatics of the in the three samples was 0.5 per cent (range, 0.2—0.9), anterior part of the diaphragm drained cranially into 0.6 per cent (range, 0.3—1.1),and 0.8 per cent (range, 0.5— parasternal lymph vessels, and the lymphatics of the 1.2), respectively. posterior part of the diaphragm drained caudally into The topography of the thoracic duct was then clarified retroperitoneal lymph vessels (Fig. 1). Often small, in by an injection of Thorotrast in a retrograde direction tercostal lymphatics were seen draining the dorsal, lateral through the catheter (Figs. 6, 7). The contrast medium part of the diaphragm (Fig. 2). In a few cases mediastinal easily passed down to the cisterna chyli and also filled lymph vessels drained the central part of the diaphragm some of the intestinal lymphatics. No valves were en (Fig. 3). countered in the duct, and no connections to the other The paired parasternal lymphatics were always seen, lymphatics in the thorax were seen. The diameter of the usually as one trunk on each side of the sternum. Some thoracic duct varied between 0.5 and 0.9 mm., with a mean times the trunk divided into two vessels on one side. The of 0.7 mm. diameter of the parasternal lymphatics varied between On the radiograms following intraperitoneal injection, 0.1 and 0.9 mm., with a meanof 0.3. The right para the organs containing cells belonging to the reticuloen vertebral lymphatic was seen in about three-fourths of dothelial system—i.e., liver, spleen, and suprarenal glands the animals. The corresponding vessel on the left side —were usually filled with Thorotrast (Fig. 1). These was filled only in one-third of the animals. The para organs seemed to be opacifled to the same extent, even vertebral lymphatics, which were filled from the small when the lymph was drained from the thoracic duct. intercostal lymphatics (mean diameter, 0.2 mm.), had a At autopsy large amounts of turbid fluid were usually diameter between 0.1 and 0.7 mm., with a mean of 0.3 mm. found in the peritoneal cavity. Otherwise no gross lesions The mediastinal lymphatics, which were seen in about were noted. Microscopic examination of sections re one-fifth of the animals, were usually single and had a vealed large deposits of Thorotrast in the lymph nodes, diameter of 0.1—0.3mm., with a mean of 0.2 mm. The especially in the mediastinal and cisternal nodes and es retroperitoneal lymphatics were always visualized on the pecially in the cortical sinuses. Large amounts of Thoro left side but were filled on the right side only in three trast were also found in the liver, spleen, and adrenals. fourths of the animals. The diameter of these vessels was Small amounts of Thorotrast were found in the kidneys, 0.2—0.6 mm., with a mean of 0.3 mm. as a rule in the glomeruli. The parasternal lymphatics, as a rule, show the highest density. In fact, the density was higher in these vessels DISCUSSION than in the thoracic duct after retrograde injection of 20 The oily lymphatic pathway from the peritoneal cavity per cent Thorotrast, indicating that the contrast medium which has been demonstrated by earlier investigators (2, had been concentrated in the lymphatics. The medias 3, 22) is the parasternalsystem. Our examinationhas tinal, paravertebral, and retroperitoneal lymphatics usu revealed several other pathways going in a cranial, as well ally seemed to be of lower density than the parasternal as in a caudal, direction. All the lymphatic pathways lymphatics. which have been revealed are shown in the schematic The parasternal, paravertebral, arid mediastinal lym drawings in Charts 1 and 2. The difference between our phatics emptied into the mediastinal lymph nodes in the examination and the earlier studies might be due to better upper part of the chest (Fig. 2). These nodes were filled radiographic technic. with Thorotrast on both sides in all the animals. The left The parasternal lymphatics probably represent the most and right retroperitoneal lymphatics drained into cisternal important drainage of lymph from the peritoneal cavity, and intestinal lymph nodes, respectively.