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Observations on the general and regional anatomy of the human liver.

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OBSERVATIOKS ON THE GENERAL AKD REGIOSAL
ANATOMY O F T H E HITMAS L I V E R 1
HAKS ELIAS
Department o f A n a t o m y , The Chicago Medical School
SEVENTEEN FIGURES
Recent studies 011 the gross anatomy of the human liver
(Elias and Petty, '52) showed that a perfect coordination of
branches of the portal veins, of the hepatic artery and of the
hepatic duct into the so-called portal triad exists only in the
peripheral portions of the liver. Near the hilum, along the
entire extension of both trunks of the portal vein and for
a distance of 5mm to 2cm along the proximal parts of the
rami and ramuli veiiae portae, no coordination of the three
systems exists.
The portal venous tree forms a rather constant pattern
subject only to miiior individual variations. However, the
branches of the hepatic artery and those of the hepatic duct
are in their arrangement strikingly different from individual
to individual. From the standpoint of surgery, this fact is
unfortunate. For it would be desirable to establish the location of the arteries and portal veins by pre-operative cholangiography. This, however, is possible only in the outlying
regions of the liver. Rami of the arteries and ducts, like the
tendrils of a vine, reach the rami of the portal vein, but they
arrive there from many different points of origin. The vascular patterns (disregarding the hepatic veins) of several
human livers may be compared with the following analogy:
near each one of several identical trellises, two branching
vines are growing (fig. 1). The identical trellises represent
the intrahepatic portal venous system of several individuals. The vines represent the hepatic artery and the hepatic
l S u p p o ~ t e dby a grant from the U. S. Public Health Service.
377
378
HANS ELIAS
duct. The vines branch irregularly and the course of their
branches cannot be predicted. They may grow directly to the
nearest lath of the trellis or they may bend and cross one
another before reaching the trellis. Thus the lower portions
of each group are quite different from one another, but the
Fig. 1 Diagram to demonstrate the iiitrahepatic portal venous systcin presenting a rather constant “skeleton” f o r the liver. It is symbolically represented a s a trellis. The hepatic arteries and the hepatic ducts (shown a s vines)
a r e independent of this portal trellis and of each other i n the proximal territories.
B u t in the distal parts, there is perfect coordination of the portal triad.
upper portions of the trellises are uniform. Each lath is accompanied by one or more branches of each plant and these
branches are closely applied to the laths (fig. 1).
Tliese observations appeared to contradict the general experieiice gained in histology where one can always observe
the rigid coordination of the portal triad. It appeared necessary, therefore, to find the histological relationships existing in the regions of gross anatomical irregularity. I n the
course of these studies a few unexpected general rules could
BEGIOSAL AKATOMY O F THE LlVEIi
379
be established concerning liver anatomy, not only dealing with
the arrangement of vessels and ducts but also concerning the
extent of the limiting plate and the poiis hepatis.
MATERIAL AND METHODS
Eight embalmed human livers were obtained from the dissecting rooni. These were selected for variations in external
morphology. Cases of complete separation (from the dorsocaudal aspect) of the left from the quadrate lobe were compared with various degrees of development of the pons hepatis.
The livers were photographed in toto. Subsequently, large
slices of liver, perpendicular to the dorso-caudal surface and
transverse to the major portal vein of the region, were taken
from each specimen at tlie following locations :
1. P a r s umbilicalis trunci sinistri venae portae - one piece
when the ligamentum teres was fully exposed, and two
01' three pieces in cases of a pons hepatis.
2. P a r s transversa trunci dextri venae portae.
3. Venae portae ramus cranialis aut superior lobi sinistri,
proximal.
4. Venae portae ramus cranialis aut superior lobi sinistri,
2 ern above point of origin.
5. Ranius lateralis, 1 J c m above point of origin.
6. In addition, a loiigitudinal slice was taken near the
mouth of the vena dextra.
Norrienclature from Elias and Petty, '52.)
The slices were labeled and photographed for identification
purposes. Then they were embedded in celloidin, sectioned at
30 p and stained with Iiernatoxylin and counterstained very
lightly with eosin. In addition, the vinylite casts used f o r a
previous study were 1-e-examined.
OBSERVATIONS
Vascular c o o r d i m t i o i z as related t o syizcles~?ao-pare.12chymal
I n all those regions where gross irregularity
exists, the vessels and ducts a r e surrounded by large masses
of connective tissue which are openly connected with the capenvironnz ent.
380
HATU’S ELIAS
sule. Figure 4 shows a section of a region of this kind at the
base of the ramus cranialis aut superior lobi sinistri.
I n all those regions where well coordinated portal triads exist, the vessels are surrounded by liver tissue on all sides. Figure 5 shows a section cut 2 em distal from figure 4. Slightly
above tlie point where good coordination of the portal triad
Fig. 2 Stereogram to show the relation of Glisson’s capsule to the portal
canals and t o the liver parenchyma. Lack of coordination of the portal triad
proximally (right). Perfect coordination distally (left). The line separating the
parenchyma (shaded) from the connective tissue (stippled) is the limiting plate.
There is but one continuous periportal-subcapsular limiting plate.
begins, tlie two big lips of liver tissue shown in figure 4 have
united. The portal canal is totally surrounded by liver tissue. Figure 6 shows a section of the portal canal of the
ramus lateralis dexter about 14 ern above its origin, i.e., just
a little above the beginning of portal triad coordination. This
canal is surrounded by liver tissue on all sides. More distally, increasingly slender, cylindrical masses of connective
REGIONAL A N A T O M Y O F THE L I V E R
381
tissue surround the vessels and ducts. This continuation of
the external capsule (tunica liepatis ex peritoiico oriunda,
Glisson) called vagina Portae (or capsula communis Portae
renae et pori biliarii by Glisson, 1654) into tlie interior of
Fig. 3 Portal vascularization of tlie territory near large “conducting” veins.
A - Ramus lateralis : B -Ramus lateralis: C -Ramus cranialis a u t superior
lobi sinistri. W, X, Y, Z : small, distributing veins. (Drawings from vinylite
casts.)
382
H A S S ELIAS
the liver tissue constitutes a portal canal. Figure 2 shows
the gradual transition of Glisson’s capsule into an intrahepatic
portal canal.
I t has been reported in 1949 (Elias, ’49) that the larger
portal vein branches do not send afferent (inlet) venules
directly into the parenchyma. These larger branches, named
“conducting veins” give rise to “small, distributing veins”
which run alongside the conducting veins. From these small,
distributing veins, inlet venules arise penetrating into the
parenchyma. The re-examination of previously used vinylite
casts revealed that the trunci venae portae, the named rami
as well as the proximal 1-2cm of the branches of the rami
are all “conducting veins. ’ More distally they may become
“axial, distributing veins,” i.e., they run in the axes of portal canals and give rise to inlet venules all along their course.
India ink injections show that the diameter of the largest
axial distributing veins is 280 p. The smallest purely conducting veins measure 400 p. Branches of intermediate caliber
show mixed character.
Figure 3 ( A and C ) shows a few small, distributing veins
arising from the ramus lateralis and from one of its side
branches (3, A ) and from the ranius cranialis aut superior
lobi sinistri (3, C). While in most small, distributing veins
the bloodflow is in the direction of that in the conducting vein
( Y ) , in many cases the small, distributing veins course transversely and slightly backward ( W ) or in the exactly opposite direction to the conducting vein (X). There are also
places where the parenchyma next to a conducting vein is
vascularized by little axial, distributing veins which arise
from somewhat larger axial, distributing veins a certain distance away from the conducting vein but course toward it
(fig. 37 B).
The lkniting plate. Remak (1855) described an epithelial
sheet surrounding the portal canals, consisting of a simple
layer of hepatic cells. This sheet was later called the limiting plate (lamina limitans). Bagley and Grafflin ( ’ 5 3 ) reported that they had found in experimental animals a limiting
REGIONAL ANATOMY O F T H E L I V E R
383
plate also under the external part of Glisson’s capsule. Since
the connective tissue of the capsule sinks with the ducts and
vessels gradually into the mass of liver, one can also say inversely, that the connective tissue of the portal canals extends
into the external capsule of the liver.
It can, therefore, be expected that tlie limiting plate of each
portal canal, since it separates the connective tissue from the
hepatic tissue, accompanies the syndesmo-hepatic boundary
throughout the extent of Glisson’s capsule and of its intrahepatic extensions, the portal canals. This expected continuity is illustrated in figure 2. Sections verify this assumption.
Figure 12 shows a section through the ligamentuni teres. Its
boundary toward the liver tissue appears as a sharp line.
Higher magnification reveals this line to be a plate of liver
cells, one cell thick. It is a typical limiting plate. The limiting plate can be followed along the entire visceral boundary
of the ligamentum teres and is seen to be continuous with the
outer surface of the liver (fig. 12). The same continuity can
be seen in figure 4 near the base of the ramus superior lolni
sinistri.
Figure 8 is a section of the ligamentum teres of a specimen which showed, externally, a pons hepatis. However, it
is evident that the ligamentum teres is continuous with the
outer capsule by means of a thick connective tissue lamina.
The limiting plate is seen to be continuous along the entire
syndesmo-hepatic boundary, i.e., from the capsule (below) via
the wall of the ligamentum teres (triangular space in the center) to the portal canal surrounding one of the ranii quadrati
(below the right extremity of the triangle). A detail of this
continuity is seen in higher magnification in figure 7. The
continuity of the limiting plate in the fissure between tlie left
and quadrate lobes is seen in higher magnification in figure 9.
Figure 6 shows the continuity of the limiting plate of the
large portal canal near the base of the ramus lateralis with
that of a small portal canal a t the riglit. This figure, as well
as figure 7, shows that the relationship of smaller portal ca-
384
H A N S ELIAS
nals to the next larger ones is very similar to that of the
large portal canals to the external part of Glisson's capsule:
there exists a thin, band-like connection of both canals, as if
the smaller one were suspended by a small ligament with the
next larger one for a certain distance. (Compare figs. 6 and
7 with the center slice in fig. 2.)
Such flat connective tissue connections have been observed
between named rami and branches directly arising from them.
Among branches of higher order (branches of branches of
named rami and smaller) such band-like connections were not
found. These connections may be compared with the webs
between the toes of frogs. Also among the bases of large
hepatic canals, surrounding tributaries of hepatic veins, similar connecting ligaments were found. Figure 15 shows the
connection by a band of the adventitiae of two hepatic veins
(the venula hepatica cranialis aut superior sinistra) and a
large tributary. These veins are likewise surrounded by a
limiting plate ( parahepatic limiting plate, Elias, '49).
From all these sections it can be seen that the external,
subcapsular limiting plate (fig. 10) is continuous with the
limiting plate at the bottom of indentations (figs. 4, 8, 12),
that this deep, subcapsular limiting plate is continuous with
those of the large portal canals (fig. 7), that the limiting
plate of the large portal canals is continuous with those of
the smaller portal canals (fig. 6 ) , and so forth. I n addition,
the limiting plate surrounding the hepatic veins is continuous with the external, subcapsular limiting plate. I n other
words: all limiting plates in one liver are continuous with
each other. This means that there is but one limiting plate
in and around an entire liver. And, since the limiting plate
is continuous with the intralobular liver plates (laminae hepatis, Elias, '49) and these are continuous with one another,
one can, without exaggeration, state that the entire normal
human liver consists of one liver plate only.
Bagley and Grafflin ('53) reported the astonishing observation (in fresh, Auorescin excreting animal livers illuminated
R E GIONAL ANATOMY O F T H E LIVER
385
with ultraviolet light) of layer upon layer of liver plates
parallel to the capsule. The existence of such multiple, parallel, subcapsular liver plates could also be observed at a few
isolated places in liuman livers. U p to 5 such layers could
be found. Figure 11 shows three layers. Sublimiting plates
were also found near some large portal and hepatic canals.
Figure 15 shows such a two-layered arrangement along the
connecting ligament at the bifurcation of a hepatic canal. The
origin of this layer arrangement, perhaps, iiiay be attributed
to compression of the wall work of liver plates near the
syndesmo-hepatic boundary. In fact, transition of “normal”
liver structure to a succession of sublimiting plates can be
observed. I n extreme cases all parenchymatous bridges between the limiting and sublimiting plates may disappear (fig.
E),but it must be emphasized that layers of sublimiting
plates occur in man in only a few isolated places.
The pon s hepotis. In most human livers, the left and quadrate lobes a r e completely separated posteriorly. Figure 1 2
shows a cross section of the ligamentum tei-es of a liver with
dorso-caudally clearly separated left and quadrate lobes. Only
a delicate connective tissue bridge connects them.
Figure 8 shows the same region in a specimen exhibiting
a narrow, externally visible pons hepatis (dorsal bridging
of the ligamentum teres). However, a microscopic examination reveals (fig. 9) left and quadrate lobes a r e not really
united, but a band of connective tissue separates the two
lobes. I n figlire 13, taken from another specimen, one sees
a wedge of quadrate lobe attached to a connective tissue
bridge. Some ducts are seen in the bridge. Two cases of
this kind have been observed.
A great degree of union exists in figure 14. The specimen
is a n enlarged, f a t t y liver. The f a t t y change was mild and
non-cirrhotic. The pons hepatis is complete. Left and quadrate lobes a r e fused together. However, in spite of parenchymal continuity, a suture like plane of demarcation and a n
external depression can be seen between the two lobes. One
has the impression that the parenchymal union across the
386
HSSS ELIAS
pons hepatis is, in this case, the result of secondary fusion
which has occurred during later life by expansion of the liver
and consequent approxiniation of both lobes.
I n two cases the pons liepatis was a complete union of left
and quadrate lobes with no recognizable line of deniarcatioii,
either external or internal.
E x t e n t of t h e zones of t h e hepatic lobules. The hepatic tissue is conventionally divided into paraportal, intermediate
and “central” zones. Though the liver lobules have recently
been shown not to be stable, anatomical entities (Elias and
Sokol, ’53), under normal blood pressure conditions lobules
are convenient territories. In order to account f o r the possibility of lobular inversion, it may be better to substitute
the term “parahepatic” for “central,” since under certain
abnormal blood pressure conditions, portal lobules appear
which have portal canals in their centers.
It is interesting to establish the extent of the three zones.
Normally, the three zones are indistinguishable from one another, but under pathological conditions, they may become
obvious. It is relatively easy to identify the parahepatic
(“central”) zone in cases of central, fatty degeneration,
though not always is the degenerated area as clearly marked
as in the specimen shown in figure 16. Figure 16 shows the
paraportal zones to be of varying width. A reconstruction
from serial sections of this specimen (not shown) dcmonstrated that the parahepatic zone invests the tributaries of the
hepatic veins with a continuous coat following their branching. Yet, at a few places, such as at the lower right in figure 16, the intermediate zone may touch the adventitia of a
hepatic vein.
I n one dog injected intravenously with indigo carmine, no
biliary excretion took place in the paraportal and in the parahepatic zones, but all the bile canaliculi in the intermediate
zones of the entire liver contained the dye in high concentration (fig. 17). No attempt is made to explain the lack of
fuiictioning of the dye excreting mechanism in the paraportal and parahepatic zones in that particular case. However,
REGIONAL ANATOMY O F THE L I V E R
387
it could be learned from this isolated specimen that, a t least
for this specimen, all the intermediate zones of the entire
liver form one continuum, appearing in sections at extremely
low magnification as a continuous pattern of faint polygons
(fig. 17). At isolated locations, the intermediate zone may
touch the adventitiae of a hepatic vein (fig. 16).
Paraportal and intermediate lesions are generally too diffuse to give accurate information on the extent of these zones.
I n cases where the intermediate zones form one polyhedral
continuum, one can conclude that the paraportal and the parahepatic zones are separated from each other by the intervening intermediate zone.
This zonal arrangement exists only under normal blood
pressure conditions. I f the portal blood pressure is lowered
or the hepatic blood pressure is elevated as is sometimes the
case in pathological conditions and in certain animals in
physiological conditions, the parahepatic zones broaden and
join laterally forming a polyhedral pattern (Elias and Sokol, ' 5 3 ) .
SUMMARY
The branches of the hepatic artery and of the hepatic duct
undergo very great variations in their arrangement in a territory a t the porta hepatis, along the trunci and about the
bases of the rami venae portae. This irregularity exists
where the perivascular connective tissue broadly comniunicates with the capsule. Regular portal triads exist more distally, i.e., in all such locations where the portal canals are
completely surrounded by liver tissue.
One continuous sheet of hepatic cells, one cell thick, the limiting plate, accompanies the entire outer and inner syndesmoliepatic boundary.
A pons hepatis can consist of extreme approximation of
left and quadrate lobes with a layer of connective tissue
between them: or of a connective tissue bridge: or parenchymal union may exist in which a suture-like plane of demarcation and an external furrow is seen between both lobes.
35s
HANS ELIAS
Finally complete parenchymal union may occur without any
internal or exteriial demarcation.
The “ceiitral” zones of all hepatic lobules form a continuous, cyliiidrical investment of the hepatic veins braiicliiiy
with theiii. The intermediate zones form a multi-polyheclral
continuum throughout the liver separating the paraportal
froiii the paraliep ;I t’ic zoncs.
L I T E R A T C R E CITED
BAGLET,
ELIZABETH,
A N D ALLANGRAFFLIN 1933 The meclianism of biliary eycretion in mammals. “Livcr I n j u r y ” Transactions 11th conference,
Macy Foundation, New York, 1953, ed. by F. W. Hoffbauer, 200-215.
ELIAS,HANS 1949 A re-examination of the structure of the mammaliaii lirrr.
11. The hepatic lobule and its relation to the vascular and biliary systems. Am. J. Anat., 85: 379-456.
E L I A S , €TANS, AND D A V I D P E T T Y 1952 Gross anatomy of the blood vessels and
ducts within the human liver. Am. J. Anat., 90: 59-111.
ELIAS,HANS,I ND ALBERT SOKOL1933 Dependence of the lobular architecture
of the liT er on the porto-hepatic blood pressure gradient. Auat. Rec.,
1 1 5 : 71-86,
GLISSON,
FRANCIS
1654 Aiintomia Hepatis, London.
RENAK,ROBERT 1805 Cntersuchungen uber die Entwicklung des Wirbeltieres,
Eerlin.
PLATE 1
EXPLANATION O F FIGURES
(The scale is valid f o r figs. 4, 5, 6, 8, 1 2 and 14)
4
Base of ramus cranialis a u t superior lobi sinistri.
5
The same ramus 1+ern distally from figure 4.
6
Ramus lateralis and side branch (right).
REGIONAT> ASATO3lY O F THE L I V E R
PLATE 1
H A N S E JJ A S
389
PLATE 2
EXPLANATION OF FIGURES
7
Connection of the portal canal enveloping one of the rami quadrati (below)
with an extension of the ligamentum teres. X o t e the coiitinuity of thc limiting plate (detail from fig. 8).
8
Same section a s figure 7. Ligainentum teres. Quadrate lobe (lower right)
touches left lobe.
9
Detail of figure 8, below. Fissure seperating left from quadrate lohe. Note
subcapsular limiting plate.
10
Subcapsular limiting plate.
11 Two layers of liver plates parallel t o subcapsular limiting plate.
1 2 Ligamentum teres of a specimen in which the left and quadrate lobes are
clearly separated, but a thin connective sheet bridges the interlobular fissure.
390
PLATE 2
REGIONAL ANATOMY O F THE LIVER
HANS ELIAS
391
PLATE 3
EXPLANATION O F FIGURES
13
A bridge of connective tissue (lomer left) attached to tlic quadlate lobe
(right).
14 Pnrencliynial pons hepatis in a f a t t y liver. A suture between left (left) ant1
cp:idr:ite (riglit) lobes call still be seen :IS \re11 as :in external iiident:ition,
i n spite of parenchymal continuity. I n the upper part of the figure one sees
the 1ig:rmentum teres containing the pars umbilicalis truiici sinistri veiiiie
poitae and the origin of the ramus intcrinedius lobi sinistri.
13
Tlic rciiuln liepatica emni:ilis a u t superior siiiistra (below) and a tributary.
A connective tissue band connects both hepatic c:inals. They are surrouiidcd
I)? the 1miliepatic limitiug plate. A t the right side near the connecting
band a double limiting plate is seen.
16
Ceiitral, f a t t y degeneration indicating the extent of the “central”
Iwpatic) zoiie.
392
(= pni:r-
R E G I O N B L ANATOMY O F T H E L I V E R
PLATE 3
HANS ELIAS
393
PLATE 4
REGIONAL ANATOMY OF THE LIVER
HANS ELIAS
1 7 Liver of dog. 60 mi" of co~iceiitratcd solution of indigo cnmiine ~ w u einjwtcil intr:rvenously a t the rate of 1en<" every two minutes. A t tlie end of two hours, the dog \KIS sacrificed. The liver was fixed in absolute alcoliol; indigo eariiiinc I l a d bcen rscwtcd in the
intermediate zones only. Very low poww pliotomicrograph sliomiiig the contincity of tlic
intermediate zones.
394
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