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*Fundad4o Gon(Alo M.1Oniz, Sal(Ador, Bahia, Brazil Br. J. exp. Path. (1981) 62, 480 HEPATIC EOSINOPHIL GRANULOCYTOPOIESIS IN MURINE EXPERIMENTAL SCHISTOSOMIASIS MANSONI R. BOROJEVIC*t, S. STOCKERt AND J. A. GRIMAUDt Fro0m the tinstitot Pasteur de Lyon, ERA 819, 77 Rue Pasteur, 69007 Lyon, France, and *Fundad4o Gon(alo M.1oniz, Sal(ador, Bahia, Brazil Received fo)p)ublicationlMay 27, 1981 Summary.-In livers of mice with acute schistosomiasis eosinophil granulocyto- poietic folliculi are described. Exogen stem cells were observed in hepatic sinusoids. Their proliferation and progressive maturation are described. Specific reactions to the presence of worms and their eggs, and Kupffer-cell stimulation and hyperplasia are considered to be responsible for this extramedullary granulocytopoiesis. AN INCREASE in the level of eosinophil Warren and Johnson (1967) and by granulocytes in blood, bone marrow and Bogitsh (1971), but the question of their involved tissues is characteristic of many origin was not solved. parasitic infections. It is particularly 3. In the hepatic parenchyma, inde- prominent in those in which parasites pendent of portal spaces and of periovular inhabit the circulatory system, or in which granulomas, folliculi can be observed, their life cycles include the passage of composed of mature eosinophils, together larvae through the host tissues (Basten, with immature forms and blastic cells. In Boyer and Beeson, 1970; Colley, 1972). earlier works, Goennert (1955), Grimaud Related to the presence and quantity of and Borojevic (1972) and Byram et al. parasite antigens in situ, eosinophilia is (1978) have interpreted these hepatic particularly high in the acute phase of folliculi in murine schistosomiasis as sites human (Diaz-Rivera et al., 1956) and in of local granulocytopoiesis. experimental (Colley, 1972; Byram, Extramedullary eosinophil granulocyto- Imohiosen and von Lichtenberg, 1978) poiesis occurs in some eosinophil leuk- infection by Schistosoma mansoni. aemias (Gross, 1962; Anteunis et al., 1978), In the acute phase of murine S. mansoni in young thymus (Bhatal and Campbell, infection eosinophil granulocyte infiltra- 1965; Sin and Saint-Marie, 1965) and, as tion is 3-fold: postulated by Dzury and Cohen (1958), in 1. In periportal spaces eosinophils form inflammatory reactions. Ultrastructural part of the inflammatory infiltrate. features of hepatic granulocytopoiesis 2. In the inflammatory granulomatous during the foetal period have been fol- reaction which forms around schistosomal lowed by Zamboni (1965), Fukuda (1974) eggs, the presence of eosinophils is related and Enzan et al. (1978). to the degree of maturation of the egg: The morphology of cells implicated in they are particularly abundant in the ectopic extramedullary eosinophilic "mixed inflammatory reaction" (von granulocytopoiesis observed in experi- Lichtenberg, 1962) where they outnumber mental murine schistosomiasis, their other types of cell. The presence of origin and their relationship with the immature eosinophils in schistosomal hepatic tissue, are the object of the present granulomas was described by Stenger, report. Corriesponrden e to: Prof Radox an Borojexik, D)epartamento (le Bioquimica, Instittuto dle Qu'imica Universidade Fe(leral (lo Rio cle Janieiro, 21910 Ilha (lo Ftun(lio, Rio (1e Janeiro, Brasil. HEPATIC GRANULOCYTOPOIESIS IN SCHISTOSOMIASIS 481 MATERIAL AND METHODS plasmic rim and flattened processes ex- Twenty inbred C3H rnice and 40 Swiss tending into the sinusoidal lumen, and Albino TO mice were exposed as sucklings to their cytoplasm was locally crowded with transcutaneous penetration of 50 cercariae of phagosomes, in which schistosomal pig- the FS strain (Bahia, Brazil) of Schistosorna ment and cell debris could be recognized. mansoni. The animals were killed after 60 days Cytoplasmic granules, corresponding to of infection. Small fragments of liver tissue were lysosomes and secretory granules, were fixed in 4%o buffered formalin for optical micros- copy, and treated by conventional histological abundant. methods. For electron microscopy, 10% Os04, Exogenous cells were mostly typical buffered in sodium cacodylate (015M) was used. mature blood leucocytes. Occasionally we Fixation was carried out at 4° for 60 inin. observed small cells with a very high Embedding was carried out writh Epoxy resin. Ultra-thin sections were made with a Reichert nucleo-cytoplasmic ratio, with subspheri- OM U2 mnicrotome, contrasted with uranyl- cal nuclei and cytoplasm rich in ribo- acetate/lead citrate solution and observed on the somes, but devoid of any particular in- Plilips EM 300 microscope. clusions or cytoplasmic differentiation. They had the characteristics of blastic cells, RESULTS but at this stage their precise identity was In acute mutine schistosomiasis eosino- difficult to tell. philic granulocytes were found in hepatic Small groups of these blastic cells were parenchyma as a diffuse infiltrate, or observed within the sinusoidal lumen, in forming large distinct folliculi. Serial close relation to the endothelial lining. In sections were studied in this work, to other places, the endothelial lining was avoid the possible influence of neighbour- interrupted, and blastic cells, together with ing inflammatory portal spaces or peri- occasional Kupffer cells, could be observed ovular granulomas. Only those fragments within Disse's space, in direct contact in which the vicinity of these inflam- with hepatocytes (Figs lb and 3). matory structures was eliminated were taken into consideration. Intraparenchymal folliculi These were observed most often in Hepatic parenchyma spaces corresponding to obliterated In our model of acute murine schisto- sinusoids. When small, folliculi did not somiasis the hepatic parenchyma pre- alter the trabecular organization of served its lobular architecture and the hepatic parenchyma, but when they were hepatocytes their trabecular organization. composed of several hundreds of cells they Hepatocellular irritation was indicated by could locally alter the normal hepatic an unusually high number of binucleate structure (Fig. 2a). cells, by the abnormal size and shape of Folliculi were composed of cells which the nucleoli and by dense, large mito- could be easily recognized as myeloid cells chondria, sometimes containing cristalloid of eosinophil granulocyte lineage. They bodies. Hepatocellular necrosis was not were remarkably closely synchronized in seen. their maturation and only exceptionally, in large folliculi, could very young cells be Hepatic sinusoids found together with mature eosinophils. The composite origin of these folliculi was These were loaded with cells. This was apparent. Three main categories of cells due simultaneously to an intense hyper- plasia of Kupffer cells and to infiltration could be recognized in folliculi: by exogenous cells. Kupffer cells had nuclei similar to those seen in endothelial Stage I cells cells, being irregular in shape and devoid Spherical or ovoid, these cells measured of nucleoli. They had a narrow cyto- 6-10 Htm in the largest diameter and had 482 R. BOROJEVIC, S. STOCKER AND J. A. GRIMAUD W: 4.7 la b- FIG. 1 Liver in acute murine schistosomiasis: intrasinusoidal formation of granulocytopoietic folliculi. (a) Semi-thin sections. x 333. (b) Electron micrograph showing Kupffer cells (K) and young eosinophil granulocytes. x 3078. HEPATIC GRANULOCYTOPOIESIS IN SCHISTOSOMIASIS 483 ,4stSi . ;<J=* FIG. 2.-Hepatic granulocytopoiesis in acute murine schistosomiasis. (a) Large mixed granulocytic follicle. Note the presence of Kupffer cells (K) and reticulin (R) in the location corresponding to Disse's space. x 2767. (b) Granulocytopoietic follicle composed of Stage I cells. x 7132. 33 484 R. BOROJEVIC, S. STOCKER AND J. A. GRIMAUD Ntw FIG. 3.-Hepatic granulocytopoiesis in acute murine schistosomiasis. (a) Granulocytopoietic follicle composed of Stage I and Stage II cells (x 5207). (b) Granulocytopoietic follicle in the intra- sinusoidal position, composed of Stage II cells. x 5180. (c) Eosinophil Stage II cell (myelocyte): Golgi zone with formation of eosinophil granules. x 21,082. HEPATIC GRANULOCYTOPOIESIS IN SCHISTOSOMIASIS 485 I~ ~~ #ltt 7 ;8s ; r2s2.>tge 7|'.e *8* v%sei FIG. 4.-Hepatic granulocytopoiesis in acute murine schistosomiasis. (a) Stage III follicle: note the continuity between the follicular space and the adjacent Disse's space. x 7375. (b) Mitosis in the Stage III eosinophil granulocyte. x 7375. 486 R. BOROJEVIC, S. STOCKER AND J. A. GRIMAUD nuclei with small indentations, slightly At their periphery folliculi were in direct condensed perichromation and an eccen- contact with hepatocytes. At the interface, tric nucleolus. Numerous polyribosomes, hepatocytes were flattened, without any scattered cisternae of rough endoplasmic sign of irritation or reaction to the pre- reticulum and a few small mitochondria sence of myeloid cells. Collagen bundles, were found in the narrow cytoplasmic rim thin and resembling the perisinusoidal (Fig. 2b). "reticulin", were sometimes observed at the periphery of folliculi. These bundles Stage II cells were topographically related to pre-exist- ing sinusoids, and no fibrotic reaction Characterized by marked differentiation, around folliculi was detected. The Disse's these were 10-13 ,um in diameter. They space of neighbouring sinusoids was in had a decreased nucleo-cytoplasmic ratio, continuity with the follicular space. with an irregularly shaped nucleus and Cell divisions were frequent in folliculi. sparse chromatin clumped along the They were not restricted to blastic cells of
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