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MICROSCOPY RESEARCH AND TECHNIQUE 38:547–551 (1997)
Introduction to The Biliary Tract, The Gallbladder,
and Gallstones
JACQUES GILLOTEAUX*
Summa Health System Foundation, Akron, Ohio 44304
KEY WORDS
biliary tract; gallbladder; nomenclature; microscopy; bile acids
ABSTRACT
This paper serves to introduce a topical section of fifteen invited original research
contributions dealing with normal and pathological development of the human biliary tract. This
section also includes comparative anatomy of the gallbladder and the cystic duct as well as, the
formation of gallstone. This series of reports have used advanced microscopic and ancillary
techniques to study adaptative changes in gallbladder epithelial cell changes regarding permeability, renewal, mucous secretion as well as cholesterol uptake and nucleation. Several contributions
deal with the blood and lymphatic drainage of the gallbladder. The gallbladder contractility is
clarified by recent findings about its innervation, elegantly demonstrated and supported by
complementary immunohistochemical and neurophysiological techniques. In vivo models for
production of cholelithiasis in the ground squirrel and the Syrian hamster are introduced. Recent in
vitro cellular and molecular models have substantially increased the understanding of biliary tract
calculi formation. Finally, a survey and new data about progesterone gene regulation of both
cholesterol metabolism and gallstone formation obtained in the Syrian hamster model are compared
with cholelithogenesis in human. Microsc. Res. Tech. 38:547–551, 1997. r 1997 Wiley-Liss, Inc.
OVERVIEW OF THE BILIARY SYSTEM
The biliary system includes the secretory units of the
liver, the bile canaliculi, bile ductules (canals of Hering), intrahepatic bile ducts, extrahepatic bile ducts,
the common hepatic duct, the cystic duct, the gallbladder, and the common bile duct. Some confusion remains
as to the terminology of the components of the biliary
system (i.e., interlobular 5 intrahepatic).
All vertebrates possess a biliary tract but not all of
them possess a gallbladder whose function as an accessory organ of the digestive system is to participate in
the enterohepatic circulation of bile (Hofmann, 1968,
1990, 1994) by storing and concentrating biliary compounds through the removal of water and the exchange
of electrolytes (Diamond, 1962; Dietschy and Moore,
1964; Wheeler, 1968). The biliary system in man includes all of the aforementioned components, although
this is not true of all vertebrates. Pfuhl (1932) reviewed
the literature and histology of the biliary system in
selected vertebrates, including humans. Morphological
aspects of the biliary system during development, differentiation (Desmet, 1994; Phillips, 1994), and histopathology (Sirica, 1995) have been reviewed recently. In
this monograph, the paper of Nakanuma et al. (1996a)
describes the normal morphology from early development to a differentiated stage of the human biliary tract
and its pathology. It has been reported that the histochemical characterization of biliary hepatic cells could
play an important diagnostic role in pathology (Strain
et al., 1995). Nakanuma et al. (1997a) have also described the extra- and intrahepatic peribiliary glands
(development, differentiation, apoptotic growth, remodeling and differentiation, immunologic functions, etc.).
These glands constitute intramural and extramural
r 1997 WILEY-LISS, INC.
mixed mucous and serous acini with the serous parts
resembling exocrine pancreatic acini (Terada et al.,
1990) that do not contain islets of Langerhans’s tissue.
This observation is particularly interesting because
Gilloteaux et al. (1995) and Oldham-Ott and Gilloteaux
(1997) illustrate that in lower vertebrates (fish) pancreatic tissue is commonly detected in the vicinity of the
gallbladder.
The bile canaliculi are formed by the adjacent plasma
membranes of the hepatocytes. This was seen by light
microscopy in 1911, and one of the first TEM studies of
bile canaliculi demonstrated this feature (Rouiller,
1956). Previously, these channels were thought to be
intercellular tubules with their own walls. Even Rouiller once believed that the bile canaliculi constituted an
incomplete barrier between the space of Disse and the
lumen of the canaliculi (Steiner and Carruthers, 1961).
It is now known that tight junctions and other specialized junctions (gap junctions and desmosomes) separate the canaliculi lumen from the hepatocytes. In an
interesting monograph of Matter et al. (1969) it is
shown that these tight junctions are efficient permeability barriers. Moreover, bile canaliculi are able to have a
coordinated contractile activity by pericanalicular, actomyosinic interactions controlled by calcium. This action
was observed in pathology (Oda et al., 1974; Oda and
Phillips, 1977) and in vitro (Oshio and Phillips, 1981, in
review by Phillips, 1994; Phillips et al., 1983; Smith et
al., 1985; Watanabe et al., 1983; Watanabe and Phillips,
1984). In addition, abundant microvilli, with varied
*Correspondence to: Dr. J. Gilloteaux, Summa Health System Foundation,
Arch Street 41, Suite 506, Akron, Ohio 44304.
Accepted 1 August, 1995
548
GILLOTEAUX
shapes and sizes, due to actin filaments remodeling
(Forscher et al., 1992) protrude into the lumen of the
canaliculi (Matter et al., 1969; Rouiller and Jezequel,
1963).
The bile ductules are circumscribed by two to four
epithelial cells, eventually becoming cuboidal, with
blunt microvilli, a basal lamina, a large spherical
nucleus, poorly developed rough endoplasmic reticulum, many free ribosomes, and few mitochondria. The
cells contact one another through complex interdigitations and have extensive tight junctions (Gabe, 1973).
The microvilli-coated intrahepatic bile duct cells
progress from a cuboidal to a columnar epithelium on a
basal lamina and they often bear a single extended
(perhaps motile) flexuous cilium ranging between 2 to
4 µm in length. An overview of the embryology, anatomy,
histochemical typing, and functioning of the epithelial
cells of the intrahepatic bile ducts (cholangiocytes) has
been performed by Alpini et al. (1994).
The extrahepatic bile ducts are composed of tall,
columnar epithelial cells, surrounded by a sheet of
connective tissue. Elastic and collagen fibers have been
observed in the basement membrane; tubular or tubuloalveolar glands, varying according to species, have also
been observed. The material secreted by the extrahepatic duct has been identified as mucin with acid
mucopolysaccharides (Gabe, 1973). A submucosa, muscularis, and adventitia are present. The extrahepatic
bile ducts join to form the common hepatic duct. This
duct connects with the cystic duct from the gallbladder
to form the common bile duct (ductus choledochus).
The common bile duct has been observed to contain
tubular glands (Spitz and Petropoulos, 1979) and PASpositive cells. The glands are more frequent in animals
without a gallbladder, such as the rat (Jones and
Spring-Mills, 1983). We refer the reader to Nakanuma
et al. (1997a) for a more detailed and recent account of
these structures. During bile formation and all along
the pathway to the gallbladder many of the cells
involved show evidence of active and passive transport
of water and electrolytes. The anatomy of the various
bile ducts differs widely among vertebrate groups.
The Gallbladder
A review of the morphological components of the
biliary tract, the gallbladder, and the formation of
gallstones across the vertebrates is offered by OldhamOtt and Gilloteaux (1997). This review shows that the
gallbladder’s microscopic architecture displays a homologic histological pattern throughout the vertebrates in
terms of layering. A lamina propria, fibromuscular
tunic, subserosal, and serosal tunics are normally
present. Small nerve ganglia and adipose tissue are
present between the fibromuscular and subserosal layers. The thickness of the gallbladder wall also varies in
vertebrates. It may be quite thick, as in many carnivores and primates, or very thin, as in the lower
vertebrates (fish, amphibians), mouse, and guinea pig.
The gallbladder’s mucosal epithelium is usually composed of tall columnar cells, displays a PAS-positive
apical aspect (in carnivores it contains lipidic inclusions),
and is coated with microvilli and other characteristics
of absorptive cells, including basolateral spaces and
digitations. Prominent junctional complexes are present
(Gabe, 1973). Bulging epithelial apices and decapita-
tions of excrescent apical structures can be found occasionally. These are more abundant in cholesterolosis
(Gilloteaux et al., 1996b), in male, in ovariectomized,
and in intact female Syrian hamster where cholelithiasis was induced by steroid hormones (Gilloteaux et al.,
1992, 1993a–c; Karkare et al., 1995; Karkare and
Gilloteaux, 1995). The same apical excrescences are
morphologically similar to the secretory endometrial
epithelial cell apices during the postovulatory phase
(Wessel, 1960; Wetzstein and Wagner, 1960; Wynn and
Wooley, 1967). This phenomenon has also been observed in fetal gallbladders (Laitio and Nevalainen,
1972) and in fish gallbladder (Gilloteaux et al., 1995;
Oldham-Ott and Gilloteaux, 1997; Viehberger, 1982).
In the surface epithelium of the mouse gallbladder,
columnar brush cells, which are possibly sensory cells,
were discovered in 1969 by Luciano and Reale and are
elegantly illustrated in this monograph, as they have
included a freeze-fracture technique (Luciano and Reale, 1997). Interestingly enough, similar brush cells
appear to be present in some amphibians and reptilian
gallbladders (Oldham-Ott and Gilloteaux, 1997).
Lamote and Willems (1997) demonstrate that the
normal gallbladder epithelium has a very low rate of
cell renewal, while mechanical distension by ligation of
the common bile duct or by neoplastic obstruction in
humans increases the mitotic activity of the tissue.
Other influences, such as hormones (caerulein, cholecystokinin (CCK)-octapeptide, CCK analogs), or a diet rich
in cholesterol and cholic acid, can stimulate high DNA
synthesis in the gallbladder epithelium. Fundusectomy
or the presence of gallstones stimulates proliferative
activity. These authors suggest that this proliferative
activity could be the result of hypergastrinemia.
Rokitansky-Aschoff crypts reaching the fibromuscular layer are present in humans. Canals of Luschka, in
which the epithelium invaginates through the fibromuscular layer and may contact blood vessels, have been
observed in humans, are well defined in the rabbit, and
almost absent in the cat (Gabe, 1973).
Gallbladder tubular and tubulo-alveolar glands,
whose presence and abundance is variable in the
lamina propria, are similar to those found in the
extrahepatic ducts. In primates, these glands are located near the infundibulum of the gallbladder, and in
ruminants they form a subepithelial layer (equivalent
to Brunner’s glands). These glands are rare in carnivores (Gabe, 1973).
Permeability
Many of the regulatory mechanisms of ion transport
across the gallbladder epithelium have been resolved
physiologically (Reuss, 1989; Reuss et al., 1991; Wheeler,
1971). Hopwood and Ross (1997) survey the permeability ‘‘barriers’’ of the gallbladder epithelium in terms of
water and ion removal. Using the mouse, they demonstrate that the gallbladder wall is able to take up
significant amounts of lipids and that inflammatory
reactions can alter membrane composition and functions. Finally, using a cationic, cytochemical probe
(cuprolinic blue; reviewed by Van Kuppevelt and
Veerkamp, 1994), Hopwood and Ross demonstrate a
significant increase of glycosaminoglycans in the basement membrane in the cholecystic gallbladder.
BILIARY TRACT, GALLBLADDER, AND GALLSTONES
Mucus
Using histo- and cytochemical lectin markers, Madrid
et al. (1989, 1994) surveyed and investigated characteristics of the glycoproteinaceous secretory products and
glycocalyx of the gallbladder epithelium across several
species, including humans. In their contribution, Madrid
et al. (1997) verify that most of the mucus is neutral,
heavily sulfated, and contains scarce sialic residues.
They also discuss the presence of core proteins which
are known molecular markers for mucus types (Audie
et al., 1993; Campion et al., 1995). Our ultrastructural
description of the human cholecystitic (Gilloteaux et al.,
1989) and cholelithiatic gallbladder shows anionic mucus secretory granules (Gilloteaux et al., 1997c). Koga
(1985) and Satoh and Koga (1997) review the pathological gallbladder storage of cholesterol in cholesterolosis.
In the case of the cystic duct, Gilloteaux et al. (1997a)
confirm the differential morphology of the gallbladder
in cholesterolosis and cholelithiasis. It is interesting to
note that LaMont (1989) has hypothesized that oxygen
radicals can stimulate gallbladder glycoprotein secretion.
Blood and Lymphatic Supply
The complex vasculature of the biliary tract and its
development is surveyed by Nakanuma et al. (1997a).
Blood supply to the mammalian gallbladder is by way of
small and medium arteries which cross the fibromuscular layer and form a fenestrated subepithelial plexus in
the lamina propria. There, blood flow could be controlled by neuropeptides, such as NPY (Gilloteaux et
al., 1990–1991). Using SEM on corrosion casts and on
KOH-macerated samples, Ohtani et al. (1997) illustrate the blood and lymphatic microvascularization of
the guinea pig gallbladder; they demonstrate that, as in
the small intestine, and in the liver lymphatics start
their trajectory as blind ends.
Innervation
Gallbladder innervation resembles that of the intestine and has been comprehensively discussed by Cai
and Gabella (1983, 1984), Goehler et al. (1988), Mawe
and Gershon (1989), Mawe (1990, 1991, 1993), Talmage
et al. (1992), etc. As reported in the monograph by
Mawe et al. (1997), the musculature and the epithelial
tissues of the guinea pig gallbladder are regulated by
small clusters of neurons which constitute a ganglionated network containing diverse important neuropeptides and enzyme markers. From a physiological point
of view, they also report that this network acts as a
complex neuromodulator, and demonstrate that hormonal CCK can access gallbladder ganglia presynaptically (no blood-barrier) to facilitate vagal terminal
release in the musculature and the epithelial layer of
the gallbladder. Splanchnic mechanoreceptors of the
biliary tract and its mesentery have been studied by
Crousillat and Ranieri (1980). Gallbladder contraction
is mediated by cholecystokinin, the cholecystokinin
antagonist pancreatic polypeptide, and others too numerous to list here (Adrian et al., 1982; Conter et al.,
1987; Spellman et al., 1979).
The presence and degree of development of a sphincter regulating the flow of bile is directly related to the
presence or absence of a gallbladder; in those animals
549
lacking a gallbladder, the sphincter appears poorly
developed (Dorst, 1973; Gorham and Ivy, 1938).
Models
In vivo models for producing cholelithiasis have also
been developed by using diverse animals (review in
Oldham-Ott and Gilloteaux, 1997). Using ground squirrels fed a high-cholesterol diet, MacPherson and Pemsingh (1996) have shown that mucus hypersecretion
occurs prior, during, and after stone formation.
Gilloteaux et al. (1996c) have shown similar changes
and stone formation after perturbing hepatic bile metabolism using female sex steroids in the male, in
ovariectomized, and in intact female Syrian hamsters
(Gilloteaux et al., 1992; Gilloteaux et al., 1993a–c;
Karkare et al., 1995; Karkare and Gilloteaux, 1995).
Medroxyprogesterone treatment alone can alter bile
and mucus composition, favoring formation of gallstones
via a down-regulation of the cholesterol 7a-hydroxylase
gene expression (Qiu et al., 1994; Gilloteaux et al.,
1997).
In vitro models are being developed to comprehend
the cell biology and pathology of the gallbladder epithelium. Nakanuma et al. (1997b) demonstrate that mucus
secretion characteristics can be maintained and studied morphologically with in vitro-grown epithelium.
Bile Acids
The concentrated bile secreted into the duodenum via
the permissive effect of cholecystokinin (Mawe et al.,
1991, 1997) provides a micellar suspension facilitating
intestinal absorption of fat soluble compounds, including vitamins (Borgström et al., 1985), as well as scavenging peroxyl radicals (Stocker and Ames, 1987; Stocker
et al., 1987a–b). In addition, bile has a laxative property due to its effect on the motility of the large
intestine (Hofmann, 1968). The composition of bile
acids in the bile varies in the animal kingdom (Haslewood, 1968; Hoshita, 1985; Hofmann, 1990, 1994; etc.):
The fish groups produce various compounds (bile alcohols in ancient fish, such as the shark), amphibians
generally produce bile alcohols, and the reptiles produce bile acids but no bile alcohols. In birds and
mammals, the type of bile acids produced seem dietdependent. Bile alcohols usually occur only in ancient
groups of mammals. Omnivores (including humans)
generally produce dihydroxy bile acids and carnivores
trihydroxy bile acids. Conjugated xenobiotics and bilirubin are other important components of bile (Arias, 1968).
In addition to bile acids, bile pigments vary with the
animal species and it is thought that gaining an
understanding of this diversity of bile pigments will aid
in comprehending altered bile metabolism in humans
(Cornelius, 1986). In plants, these pigments perform
photosynthetic functions. Bile pigments in mammals
have no known function; they are, however, potentially
toxic (Cornelius, 1986; Troxler, 1986). Further investigations in this area are clearly indicated.
Examining artificial and human native bile by cryotransmission electron microscopy, Kaplun et al. (1996)
have demonstrated that dilution induces cholesterol
supersaturation, resulting in the production of a range
of microstructures: spheroidal, uni- and multilamellar
micelles, followed by tubular and helical as well as the
classical plate-like cholesterol. This model can help to
550
GILLOTEAUX
decipher the beneficial role of bile in preventing the
cholesterol nucleation process in the gallbladder.
In order to comprehend the pathologic etiology of the
hepatobiliary system, most investigations have to rely
on case studies, or animal models and in vitro studies.
It would be interesting to obtain fresh postmortem or
surgical human specimens in order to more fully describe certain structures, such as the cystic duct
(Gilloteaux et al., 1997b), which are easily damaged
during autopsy or following fixation delays after surgical removal.
ACKNOWLEDGMENTS
I would like to thank Dr. J.E. Johnson Jr., Chief
Editor, for inviting me as Guest Editor for this special
monograph. I would also like to thank all the contributors for their efforts in providing informative and
well-illustrated manuscripts on the topic, and recognize
the experts and reviewers for their scientific assistance
and for having returned as promptly as possible the
manuscripts submitted to them. I wish, therefore, to
acknowledge Drs. Ian A.D. Bouchier, V.J. Desmet, Mr.
L.C. Gilloteaux, Drs. A. Groom, R. Hakanson, W.S.
Hawkins, M.R. Jacyna, E.R. Lacy, L. Luciano, S. Nagamori, Mrs. C. Oldham-Ott, Drs. G. Perry, E. Reale, W.
Schemann, P. Scheuer, B.A. Schulte, D.P. Siegel, R.J.
Spontak, P. Wade, and W. Willems.
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