The Fine Structure of the Terminal Branches of the Hepatic Arterial System of the Rat'

The Fine Structure of the Terminal Branches of the Hepatic Arterial System of the Rat' WILLIAM E. BURKEL Department of Anatomy, The University of Michigan, Ann Arbor, Michigan ABSTRACT The fine structure of the smallest branches of the hepatic arterial system of the rat was studied with the light and electron microscope by means of alternate thick and thin serial sections, The terminal arborizations of the hepatic artery closely follow the pattern of the portal vein and give rise to a dense network of capillaries in the periportal connective tissue which closely surrounds the bile ducts. These periductal capillaries end by join- ing (a) interlobular veins, (b) terminal distributing veins, (c) sinusoids directly or, (d) sinusoids in common with branches of the portal vein. The capillaries arising from larger arterioles have well developed precapillary sphincters at their origins, while those arising from terminal arterioles have less prominent smooth muscle cuffs. There are no smooth muscle sphincters at the terminal ends of the capillaries where they join branches of the portal vein or sinusoids. Large endothelial cells usually guard these junctions and frequently their nuclei bulge into the lumens of the vessels and may close them off. Occasionally unmyelinated nerves with vesicles about 500 A in diameter, some of which are granulated, are in close proximity to the endothelial cells of the capillaries. Endothelial cells also guard the beginnings of sinusoids originating from the portal vein. The sinusoids arising from periductal Capillaries are identical in structure to those directly off from the portal vein. Initially the sinusoids from both types of vessels are like capillaries, with a continuous basement membrane around them and an unfenestrated endothelium. A short distance into the parenchyma they lose their basement membrane, become fenestrated and are typical sinusoids. The vasculature of the liver has been Donald, '53; Knisely et al., '57; McCuskey, studied extensively during the three cen- '66). These studies have shown, in addition turies since the time of Glisson. Although to the types of connections between the a great deal of work has been done, some hepatic artery and portal vein, numerous of the finer details of the relations of the sphincter-like structures which control the hepatic arterial system to the portal venous flow of blood between the two systems. system are still obscure. These "sphincters" are assumed to be con- The interconnections between the portal tractile reticulo-endothelial or endothelial vein and hepatic artery have been demon- cells ( McCuskey, '66), but their finer struc- strated using histological sections, wax ture is unknown. reconstructions, injections, injection-corro- Fine structure studies of the liver have sion methods, roentgenography and trans- concentrated mainly on the parenchymal illumination of living specimens. Recent cells, sinusoids, and bile ducts. No defini- studies by Hase and Brim ('66) and Mitra tive work has been done on the hepatic ('66) fairly well summarize the present arterial system, its connections to the portal understanding of the distribution of the vein and sinusoids, or to the structure of hepatic artery and its terminations as seen sinusoids arising from terminal branches in static studies. The functional microcir- of the hepatic artery. The structure of si- culation of the liver, however, is a dynamic nusoids originating exclusively from portal system with higher pressure hepatic arterial veins has been studied (Burke1 and Low, vessels interconnected with lower pres- '66). sure portal veins and sinusoids and it is The work reported here demonstrates the best studied in living animals. This has fine structure of the terminal arborizations been done extensively by transillumination Received June 2, '69. Accepted Feb. 12, '70. (Knisely, '36; Block, '40, '55; Wakim and 1 Supported by a grant from the Faculty Research Fund, Horace H. Rackham School of Graduate Studies, Mann, '42; Wakirn, '44; Irwin and Mac- The University of Michigan. ANAT. REC.,167: 329-350. 329 330 WILLIAM E. BURKEL of the hepatic artery and their connections arterial branches usually accompany a por- to the portal vein and sinusoids. Particular tal vein of about 600-700 ,,. in diameter attention was given to the junctions be- (fig. 2). One of the branches (figs. 2, 3) is tween the arterial and venous systems and generally larger and it gives rise to the to the areas of the apparent sphincters. smaller ones (fig. 4). The small branches in turn give rise to rich network of capil- MATERIALS AND METHODS laries (fig. 7) found in the portal space. Twenty healthy, young adult, albino rats On the bases of their size and the struc- were anesthetized with 3.5% chloral hy- tural makeup of their vascular walls, it is drate (1 m1/100 gm of rat) and perfused convenient to describe four different types through the heart with glutaraldehyde of vessels forming the terminal parts of the (Sabatini et al., '63) or gluaraldehyde- hepatic arterial ~ystem.~Vessels approxi- formaldehyde (Karnovsky, '65) using a mately 50-100 in diameter and with a modification of the technique of Palay et wall 10-15 thick are considered to be al. ('62). Perfusion continued until a vol- arterioles. Terminal arterioles are 10-50 ume of fixative (in ml) equal to, or greater in diameter and have a wall about 5 thick. than the weight of the animal had been Vessels with diameters less than 10 p are used. Liver tissue was then removed, considered to be capillaries. The transi- minced into blocks approximately 2 X 2 X tional vessels between terminal arterioles 1 mm in size, washed in buffer and post- and capillaries, with lumens of about 10 p, fixed for two to three hours in 1% OsO, but with walls about 5 p thick are consid- containing the same type of buffer used ered to be precapillaries. in the perfusion. The tissue was dehy- drated in a graded series of alcohols con- Arterioles taining 1% phosphotungstic acid. Embed- Vessels with a caliber of 50-100 p are ment was in Epon 812 (Luft, '61) with considered to be arterioles. A large arteriole polmerization at 60°C for 24 hours. (about 100 p) typically accompanies a por- Thick sections (1-2 p) of the entire face tal vein of about 500-700 in diameter of the embedded tissue blocks were then (fig. 3). made for light microscopy and stained at The endothelium of this type of vessel 80°C with either 1% toluidine blue in 1% varies greatly in thickness depending upon borax, or Paragon Multiple Stain for Fro- the state of contraction of the arteriole. In zen Sections; also containing 1 % borax. the nuclear region the endothelium may be After examination of the thick sections, the as much as 5 thick and in other places blocks were trimmed for ultramicrotomy so only 0.2 p. The cells are joined by tight that they included a suitable portal area. junctions in the usual manner, with one Finally, alternating thin (for electron mi- cell interdigitated with or overlapping its croscopy) and thick (for light microscopy) neighbor at their point of contact. Pinocy- serial sections of the selected portal areas totic vesicles are numerous, but fenestrae were made in order to follow the branches are never seen. Microtubules and fine fila- of the hepatic artery. Thin sections were ments (50-100 A in diameter) are visible mounted on single hole grids which were in the cytoplasm. The filaments and tubules covered with formvar membranes and are not arranged in bundles, but for the stained with lead citrate (Reynolds, '63). most part are orientated with the long axis The thick sections were stained as above, of the cells. A basement membrane under- lies the endothelium separating it from the OBSERVATIONS elastica interna. The hepatic artery winds through the The elastica interna itself is not a con- portal space in close association with the tinuous layer, but it consists of a meshwork portal vein, bile ducts and lymphatic ves- of elastic fibers and microfibrils about 0.1- sels giving off numerous branches along its 2 Paragon C. and C. Company, Inc., 190 Willow Ave., course. As the portal vein branches and be- Bronx, New York 10454. 3The terminology used to describe the various ves- comes smaller the artery does also, until sels of the vascular tree is not uniform. A summary of deep within the liver it is represented only some of the terms used is found in the work of Movat and Fernando ('63). The terminology used here is sim- by arterioles and capillaries. Two or three ilar to that of Rhodin ('67). TERMINATIONS OF THE HEPATIC ARTERY 331 0.2 p thick. In vessels larger than 100 p the only a single layer of circularly arranged elastica interna is usually a complete layer smooth muscle cells. No elastica externa while in vessels of 50 p, or less (fig. 4), and little or no tunica adventitia are pres- elastic components are almost completely ent. The surrounding cells (bile duct cells, absent. fibroblasts, mast cells etc.) are tightly The tunica media of 100 arterioles is packed directly against the basement mem- about 10 thick and usually consists of brane of the smooth muscle of the media two circumferentially arranged layers of except in a few places where there are col- smooth muscle cells. Each cell is enclosed lagen fibers. These vessels appear to be in a basement membrane except at points more abundantly supplied with unmye- where the lateral cell membranes are in linated nerves than the arterioles but the contact to form a nexus (Dewey and Barr, nerves themselves are identical. ’62). Numerous fine filaments, microtu- The terminal arterioles give off numer- bules and dense bars, thought to be contrac- ous capillaries as they traverse the portal tile protein (Rhodin, ’67), are evident in space.

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