Histological damage and inflammatory response elicited by Monobothrium wageneri (Cestoda) in the intestine of Tinca tinca (Cyprinidae)

Abstract

Background: Among the European cyprinids, tench, Tinca tinca (L.), and the pathological effects their cestodes may effect, have received very little or no attention. Most literature relating to Monobothrium wageneri Nybelin, 1922, a common intestinal cestode of tench, for example, has focused on aspects of its morphology rather than on aspects of the host-parasite interaction.

Results: Immunopathological and ultrastructural studies were conducted on the intestines of 28 tench, collected from Lake Piediluco, of which 16 specimens harboured tight clusters of numerous M. wageneri attached to the intestinal wall. The infection was associated with the degeneration of the mucosal layer and the formation of raised inflammatory swelling surrounding the worms. At the site of infection, the number of granulocytes in the intestine of T. tinca was significantly higher than the number determined 1 cm away from the site of infection or the number found in uninfected fish. Using transmission electron microscopy, mast cells and neutrophils were frequently observed in close proximity to, and inside, the intestinal capillaries; often these cells were in contact with the cestode tegument. At the host-parasite interface, no secretion from the parasite's tegument was observed. Intense degranulation of the mast cells was seen within the submucosa and lamina muscularis, most noticeably at sites close to the tegument of the scolex. In some instances, rodlet cells were encountered in the submucosa. In histological sections, hyperplasia of the mucous cells, notably those giving an alcian blue positive reaction, were evident in the intestinal tissues close to the swelling surrounding the worms. Enhanced mucus secretion was recorded in the intestines of infected tench.

Conclusions: The pathological changes and the inflammatory cellular response induced by the caryophyllidean monozoic tapeworm M. wageneri within the intestinal tract of an Italian population of wild tench is reported for the first time.

Figure 1

A heavy infection of Monobothrium wageneri. (a) A heavy infection of Monobothrium wageneri comprising over 100 tapeworms in a single cluster, scale bar = 1 cm. (b) Attachment of M. wageneri resulted in the formation of a raised, rounded nodule (arrow) surrounding the worms, scale bar = 5 mm. (c) Anterior intestine of a tench, Tinca tinca, infected with M. wageneri; note the deep penetration (arrows) of the scolex and neck of worm, scale bar = 1.3 mm.

Figure 2

Transverse section through the intestine of a tench infected with several Monobothrium wageneri. (a) Transverse section through the intestine of a tench infected with several Monobothrium wageneri showing a pronounced inflammatory response surrounding the scoleces and a marked lack of epithelia at the site of tapeworm attachment (arrows). Note the presence of intact epithelia (curved arrow) in close proximity to the nodule, scale bar = 200 μm. (b) Focal attachment of several M. wageneri penetrating the intestine of a tench as far as the muscularis. An intense host cellular reaction around the scoleces is visible (arrows), M = muscularis, scale bar = 200 μm. (c) Scolex of M. wageneri (asterisk) is surrounded by numerous granulocytes (arrow heads) and collagenous fibres (curved arrows), scale bar = 50 μm. (d) A high number of mucous cells (arrows) are visible within the epithelia in the immediate vicinity of the scolex (asterisk). Note the intense recruitment of granulocytes (arrow heads) within the sub-mucosa, scale bar = 100 μm. (e) The villi adjacent to the body of the cestode (asterisk) are seen to be covered with a blanket of mucus (curved arrows) and possess a high number of mucous cells (arrows). Numerous granulocytes (arrow heads) are evident within the sub-mucosa, scale bar = 100 μm. (f) Alcian blue/PAS stained mucous cells close to the site of cestode attachment. The arrows indicate that most mucous cells stain positively for acid glycoconjugates whilst the arrow heads indicate that a lower number of mucous cells stain for the presence of mixed glycoconjugates, scale bar = 10 μm.

Figure 3

A TEM section through two mucous cells (arrows) and a rodlet cell (arrow head) within the intestinal epithelium of a tench. (a) A TEM section through two mucous cells (arrows) and a rodlet cell (arrow head) within the intestinal epithelium of a tench, Tinca tinca, infected with Monobothrium wageneri. Note that within the mucous cells there are electron-opaque and electron-lucent granules, scale bar = 4.3 μm. (b) Neutrophils (curved arrows) inside a capillary and within the connective tissue of the sub-mucosa of an infected tench. Arrow heads show the position of the mast cells within the connective tissue, scale bar = 4.4 μm. (c) Mast cells (arrow heads) and neutrophils (curved arrows) in close proximity to the scolex tegument of M. wageneri (asterisk), scale bar = 4.6 μm. (d) A neutrophil (curved arrow) attached to the scolex microtriches. Asterisk marks the scolex tegument, scale bar = 1 μm. (e) A mast cell releases its granules (arrow heads) in the vicinity of the scolex microtriches (arrows), scale bar = 0.5 μm. (f) Free mast cell granules (arrow heads) are visible among the scolex microtriches (arrows), scale bar = 1 μm.