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h a t . Histol. Embryol. 26 271-275 (1997)997 Blackwell Wissenschafts - Verlag, BerlinISSN 034 2096School of Veterinary Medicine, Hanover, G ermanyObservations on the Fine Structure of the Liver in the Camel Camelusdrom edarius)S. Lalla and W. DrornmerDepartment of Anatomy and Department of Pathology2, School of Veterinary Medicine, Bunteweg 17, D-30559 Hannover,GermanyWith seven figures

SummaryThe structure of macroscopically inconspicuous livers in 23adult camels Cumelus dromedurius) was studied by light andtransmission electron microscopy. A well-developed connec-tive tissue characterizes the camel liver. Thick trabeculaedivide the liver parenchyma into lobules. Portal tracts andcentral veins are surrounded by a variable amount of fibroustissue. In the perisinusoidal space (DISSE), collagen fibresform a dense three-dimensional network around the sinusoids.A mild to moderate fatty infiltration is present in hepatocytes ofall animals. In the epithelial cells of the bile ducts, small tomedium sized lipid inclusions are a comm on feature.The ultrastructure of hepatocytes in the camel livercorresponds to that of other domestic mammalian species.The endothelial cells lining the sinusoids show a multiplefenestration and are surrounded by a discontinuous basallamina. Fat-storing cells are numerous and contain lipiddroplets varying in size, number and electron density fromone cell to another.

ZusammenfassungZur Feinstruktur der Kamelleber Camelus drornedanusMakroskopisch unauffallige Lebern von 23 adulten KamclcnCamelus dromedurius) wurden licht- und transmissionselek-

tronenmikroskopisch untersucht. Charakteristisch fur dieKamelleber ist ein gut ausgebildetes Bindegewebe. Breiteinterlobulare Septen lassen die Lobulierung der Leber bereitsmakroskopisch erkennen. Portalfelder und Zentralvenen sindvon Bindegewebe unterschiedlicher Auspragung um geben. ImPerisinusoidalraum (Disse-Raum) bilden Kollagenfasern eindichtes dreidimensionales Netz. Eine gering-bis mittelgradige,vonviegend mittel-bis grobtropfige Lipidinfiltration ist in denHepatozyten bei allen untersuchten Tieren zu beobachten.Dagegen sind in den Gallengangsepithelien klein- bis mittel-tropfige Fettvakuolen ein hgufiger Befund.Die Ultrastruktur der Hep ato ~y ten er Kamelleber entsprichtder unserer Haussaugetiere. Die die Sinusoide begrenzendenEndothelzellen sind multipel fenestriert und liegen einerdiskontinuierlichen Basallamina auf. Perisinusoidalzelleri sindhaufig im Disse-Raum zu sehen und weisen Lipidtropfenunterschiedlicher GroBe, Anzahl und Elektronendichte auf.

Received for publication December, 1995

lntroductionThe liver of the camel shows special features compared to otherdomesticated animals. The lobulation is well marked du e to theexcess of the interlobular connective tissue (Hegazi, 1954).Because of the thick interlobular septae, the liver lobules areeven macroscopically visible. Furthermore, the borders of theliver, most markedly on the left lobe, are characterized by thepresence of num erous irregular fissures, which are continued asa network of grooves on the diaphragmatic and visceralsurfaces. A gall bladder is absent (Abdalla et al., 1971; Ouhsineand Zguigal, 1983; Smuts and Bezuidenhout, 1987). Thepresent study is supposed to supplement the data about theultrastructure of the camel liver which, so far, are very rare. Theonly reports have been given by Khatim et al. (1985), withspecial regard to the hepatobiliary system.

Fig. 1.Left hepatic lobe, visceral surface, with multiple small units.11 s. (hpyrighr Clearance Cente r Code Sta tement : 0340 2096 / 97 / 2604 0271 14.00/ 0


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272 S. L LL and W. DROMMERFig. 2. A moderate fatty infiltration ofthe camel liver: the hepatocytes containlipid droplets of varying size. The lipidcontent is not entirely preserved andappears as light vacuoles. Semithinsection, toluidin-blue, x350.

Fig. 3. Lipid inclusions (L) located in theepithelial cells (EC) of an interlobularbile duct as well as in the lumen of thebile duct. TEM, x4000

Materials and MethodsThe livers of 23 adult (about 8-15 years) Sudanese camels ofboth sexes were collected at the Cairo abattoir. For lightmicroscopy, tissue samples were taken from the left, right andcaudate lobe, fixed in 4 neutral buffered paraformaldehydeand processed by routine histological technique. Paraffinsections were stained with haematoxylin/eosin and man. APAS reaction was carried out. For identification of lipofuscin,autofluoresc ence of unstained paraffin sections as well a s theZIEHL-N EELSEN M ethod for acid-fast lipofuscin were used.Frozen sections were stained with oilred.lmmediately post-mortem, specimens for electron micro-scopy were fixed by immersion in 5% cacodylate bufferedglutaraldehyde and post-fixed in 1 osmium tetroxide. Thesamples were embedded in EPON 812. Ultrathin sections werecontrasted with uranyl acetate and lead citrate.

ResultsThe cam el liver is characterized by w ell-developed connectivetissue. Thick trabeculae divide the liver parenchyma intopolygonal lobules. Small strands o connective tissue pass fromthe interlobular septae into the lobular parenchyma. Placed inthe Disse space, the collagen fibres form a close three-dimensional network around the sinusoids. Portal tracts aresurrounded by a variable amount of fibrous tissue. Mast cellsare frequently see n in this area. Cen tral veins are surro unded bycircular arranged bundles of connective tissue, which areinterrupted for the openings of the sinusoids. The left hepaticlobe, which is macroscopically highly dissected into severalsmaller units (Fig. l), microscopically shows the largestamount of interlobular and intralobular connective tissue.The polyhedral hepatocytes either contain one spherical,voluminous nucleus or, frequently, are binucleate. The


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Fine Structure of the Camel Liver 73Fig. 4. Lipofuscin granule (LF)containing lipid droplets (L), electrondense grains and focal lamellar structures.TEM x 64000.

Fig. 5. Hepatocyte showing structurescomposed of concentric smooth lamellaecut obliquely (long arrow) andtransversely (short arrow). TEM,x25 600.

cytoplasm is slightly eosinophilic, dependin g on the amount ofglycogen, with clumps of basophilic m aterial. Frequently, finebrown granules of lipofuscin are spread in the cytoplasm.Lipofuscin granule s are the most com monly occ urring form oflysosomes in normal camel hepatocytes. Despite the macro-scopically dark brown colour and firm consistency, micro-scopically a mild to moderate fatty infiltration is present inhepatocytes of all animals. In the semithin specim ens the lipidcontent is not entirely preserved, but appea rs as light vacuoles.The affected hepatocytes show, in most cases, a single or fewlarge vacuoles, whereas some of them contain many smallvacuoles (Fig. 2). In the epithelial ce lls of the bile ducts, smallto medium sized lipid inclusions ar e a comm on feature (Fig. 3).They are lying next to the nucleus on the luminal side of thecell. Using the PAS reaction, the lipofuscin granu les can easilybe differentiated from the irregularly shaped plaques ofglycogen deposits. The amount and the distribution of the

glycogen in the livers are slightly variable. In hepatic cellsshowing lipid infiltration, the glycogen is concentrated aroundthese vacuoles. In the epithelium cells of the bile ducts, small tomedium sized lipid droplets are present. Generally, they arelocated close to the nucleus.The sinusoidal plasma membrane of the hepatocyte formsniicrovilli, which project in to the perisinusoidal space, wherethey are often surrounded by an abundance of collagen fibres.The canalicular membrane delimiting the biliary canaliculi5how5 numer ous long and broad microvilli. S ingle membr ane-bound elcctron-light vacuoles are observed in the canaliculi.The canalicular lum en is isolated from the perisinusoidal spaceby tight junctions, intermediate junctions and desmosomes.Sometimes, single membrane bound vesicles containingamorphous material are visible within the bile canaliculi. Thelateral rnembrancs of hcpatocytcs are separated by a smallintercellular sp ace. They are occasionally anchored t o each


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274 S. L LL and W. DROMMERFig. 6. Fat-storing cell, n the Dissespace, with a nucleus of triangular shape,lipid droplets (L) concentrated at one sideof the cell and slightly dilated cisternaeof the rough endoplasmic reticulumarrows) are seen. EM, ~12000

other by desmosom es and intermediate junctions. So me of theinterhepatocytic plasma membranes are seen forming cone-shaped interdigitations. Next to the sinusoidal membrme, thecytoplasm contains many sm all electron light vesicles. A well-developed rough endoplasmic reticulum appears mainly in thevicinity of mitochondria and the nucleus. It is most prominentin the periportal cells. The smooth endoplamic reticulum is

Fig. 7. The extended process of an endothelial cell E) lining thesinusoidal space S) contains multip le pores short arrow).A basementlamina long arrows) is interposed betw een the endothelia l cell and themicrovilli of hepatocytes H) in the Disse space. E M 40000 .

often found near the rough endoplasmic reticulum or mostcommonly interposed among glycogen rosettes. The Golgiapparatus is situated close to the biliary pole of the hepatocytes.Mitochondria are numerous and show few cristae and fewmatrix granules. They are closely related to rough endoplas-matic reticulum and are more concentrated near the sinusoidalsurface. The cytoplasm of the hepatocytes contains abundantaggregated glycogen rosettes, generally associated with thesmooth endoplasmic reticulum. Lipofuscin pigment granulesare round to oval, irregular in shape and consist of one ornumerous lipid droplets, electron dense grains, an amorphousmatrix varym g in electron density, and focal lamellar structures(Fig. 4). A special feature of hepatocytes of some cam els is theoccasional presence of cylindrical structures composed oflinear to oval arrays of lamellae. These multilamellar structuresmay be of endoplasmic origin (Fig. 5).Fat-storing cells are numerous and located in the Dissespace, where they are often placed in a recessus formed by twohepatocytes. Size, number and electron density of the lipiddroplets are highly variable from o ne cell to another. They canbe located on one or both sides of the irregular shaped nucleus.The cytoplasm of the fat-storing cells contains a well-developed rough endoplasmic reticulum with slightly dilatedcistemae (Fig. 6). The endothelial cells lining the sinusoidsshow multiple fenestrations and are surrounded by a discon-tinuous basal lamina (Fig. 7). Gaps occur between theendothelial cells.

DiscussionThe liver surface shows many inckurae which are most obviousin the Lobus hepatis sinister. From the thick liver capsula,trabeculae enter the liver parenchyma and delimit the liverlobules. There is a great variation in the amount anddistribution of connective tissue in the liver of different tissuesamples, although the lobus hepatis sinister always shows moreconnective tissue than the other lobes. This may be correlatedwith the numerous fissurae and lobules, which are allsurrounded by the thick liver capsulae. Fouad et al. (1984)


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Fine Structure of the Cam el Liver 275investigated the prenatal deve lopme nt of the liver, starting withfetuses of day 74. It is already on day 74 that mesenchymalcells have produced fine reticular and collage nous fibres, whichextend between the anastomosing hepatic sheets. In the adultanimal, fibrocytes are only observed in the connective tissuesurrounding the portal tracts and the hepatic lobules. In thefibrotic camel liver, transitional cells with the appearance ofboth fat-storing cells and fibroblasts are located close tocollagen fibres in the perisinusoidal space. In these cells, lipiddroplets are less numerous and reduced in size, while thenumber of cisternae of rough endoplasmatic reticulum and thedegree of swelling has increased (Lalla, 1992).The endothelium of the sinusoids in most mam mals lacks adistinct basal lamina. In the camel liver, a discontinuoussinusoidal basal lamina is present. In the liver of the sheep(Grubb and Jones, 1971; Gooneratne et al., 1980; Sauer, 1980)and the goat (Kuhn and Olivier, 1965) sinusoids werecompletely surrounded by a basal lamina. In the sheep, thesinusoidal basal lamina develops during postnatal life (Gem-me11 and He ath, 1972). Following p erfusion fixation of livers insheep (Wright et al., 19 83a) and goat (Wright et al., 198 3b), thesinusoidal lumen communicated directly with the perisinusoi-dal space via the endothelial fenestrae. Major constituents ofbasement membranes type IV collagen, laminin, and fibronec-tin are also present in the perisinusoidal space, as shown byimmunohistochemical methods (Martinez-Hernandez, 1984;Bissel et al., 1987) in norm al rat livers. Thus the presence of anultrastructurally v isible basemen t lamina in the sinusoids of thecamel liver may only be a question of concentration andarrangement of basement membrane proteins. There is noinformation whether the formation and presence of the basallamina is related to the well-developed intralobular connectivetissue in the camel liver. The transport and exchange ofsubstances between the circulating blood and perisinusoidalspace may be influenced by the presence of the partly formedbasal lamina and the three-dimensional network of collagenfibres in the perisinusoidal space.Generally, the fine structure of hepatocytes in the camelresembles that of other mammalian species. A few lipidvacuoles in normal hepatocytes are common in differentspecies. A mild to moderate fatty infiltration of the liver waspresent in all camels. Shahien et al. (1977) also found inslaughtered camels, small to medium sized lipid droplets,mainly concentrated in the peripheral part of the hepatocytes,along the sinusoids. All animals in the present study were in agood nutritional state. However, a preliminary report aboutfeeding and keeping of these animals could not be obtained.Thus , the extremely high content of lipids in all our specimensmay either be the result of fattening before slaughtering or anindication of a special fat metabolism in the camel. As in trueruminants, volatile fatty acids are produced in the camelforestomach (Holler et al., 1989), but at the sam e time camelsmaintain a high blood glucose level (Uro, 1986) that is typicalnot for ruminants but for monogastric animals. Com pared to theactivities of citrate cleavage enzyme, malic enzyme, and fattyacid synthase, respectively, in ruminant livers, the activities ofthese enzym es were much higher in the camel liver (M irgani etal., 1987 ; Uro et al., 1987). These results sugg est, that the livermay be a s important for lipogenesis in the camel.

ReferencesAbdalla, O., I Arnautovic and M. F. A. Fahmy, 1971: Anatomicalstudy of the liver of the camel Camelus dromedarius). I.Topography and morphology. Acta Morphol. Need.-Scand. 9 85-100.Bissell, D. M., D. M. Arenson,J. J. Maher and F. J. Roll, 1987: Support

of cultured hcpatocytes by a lam inin-rich gel. Evidence for afunctionally significant subendothelial matrix in normal rat liver. JClin. Invest. 79, 801-812.Fouad, S . M., A. M. El-Keshawy and A. Se lim, 1984: Histological andhistochemical studies on the prenatal development of the liver ofone-humped camel Camelusdromedarius). Vet. med. J (Cairo)32Gemmell, R. T. and T. Heath, 1972: Fine structure of sinusoids andportal capillaries in the liver of the adult sheep and the newbornlamb. Anat. Rec. 172, 57-70.Gooneratne, S. R., J McC. Howell and R. D. Cook, 1980: nultrastructural and morphometric study of the liver of normal andcopper-poisoned sheep. Am. J. Pathol. 99 4 2 9 4 5 0 .Grubb, D. J. and A. L. Jones, 1971: Ultrastructure of hepatic sinusoidsin sheep. Anat. Rec. 170, 75-80.Hegazi, A. H., 195 4: The liver of the camel as revealed by macroscopicand m icroscopic examinations. Am. J Vet. Res. 15, 4 4 4 4 4 6 .Holler, H., Q. Breves, M. Lechner-Doll and E. Schulze, 1989:Con centra tions of volatile fatty acid s and acetate production rates inthe forestomachs of grazing camels. Comp. Biochem. Physiol. 93B4 1 3 4 1 6 .Khatim, M . S., M. N. Bou-Resli, L. F. Bishay and K. A. Gum aa, 1985:Ultrastructure of the intrah epatic bile duct system of the one-h ump edcamel Camelus dromedarius) Anat. Anz. 160 251-258.Kuhn, N. 0. and M. L. Olivier, 1965: Ultrastructure of the hepaticsinusoid of the goat Capra hircus). J. Cell Biol. 26 977-979.Lalla, S. , 1992 : Untersuchungen zur Feinstruktur der Leber und zuverschiedenen Hepatop athien beim Kame1 Camelus dromedarius).Hannover, Tierarztl. Hochsch., Diss.Martinez-Hernandez , A., 1984: The h epatic extracellular matrix. I.Electron immunohistochemical studies in normal rat liver. Lab.Invest. 51 57-74.Mirgani T., A. B. 0. Uro and H. P. Sallmann, 1987: Studies onlipogenic enzymes in camel tissues. 1 Enzymes of the citratecleavage pathway. Scientific Report 1983-1987, Univ. Khartoum,Suda n, 71-77.Ouhsine, A. and H. Zguigal, 1983: La conformation extkrieure et lalobation du foie du dromadaire Camelus dromedarius), Zbl. Vet.Med. C 12,25-32.Saue r, R., 198 0: Verg leichen de Untersuchungen zur Ultrastruktur derLebersinusoide. Hannover, Tierarztl. Hochsch., Diss.Shahien, Y . M., M. F. Fahmy and S. M. Sokkar, 1977: A histochemicalstudy of the liver of normal camels. Vet. Med. J. (Cairo) 25 261-

270.Smuts, M. M. S. and A. J. Bezuidenhout, 1987 : Anatomy of thedromedary. Oxford: Clarendon Press, 129-132.Uro, A. B. O., 1986 : Carbohydrate metabolism of camels with specialreference to sources of blood g lucose. Camel Research Papers fromthe Sudan, ILCA, Addis Abeba, 28-33.Uro, A. B. O., T. Mirgani and H. P. Sallmann, 1987: Studies onlipoge nic enzym es in cam el tissues. Effect of the nutritional state onfatty acid synthetase. Scientific Report 1983-1987, Univ. Khartoum,Sudan, 85-89.Wright, P. L., K. F. Smith, W . A. Day and R. Fraser, 1983a: Hepaticsinusoidal endothelium in sheep: An ultrastructural reinvestigation.Anat. Rec. 206 385-390.Wright, P. L., J A. Clemett, K. F. Smith, W. A . Day and R. Fraser,

198 3b: Hepatic sinusoidal endothelium in goats. Aust. J. Exp. Biol.Med. Sci. 61 739-741.

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