Anguilla anguilla vs Contracaecum rudolphii: Granuloma allows host tolerance and parasite survival

High survival of the nematode Contracaecum rudolphii in European eel, Anguilla anguilla L. despite an extensive recruitment of immune cells in granulomas is described. A total of 39 eel specimens captured in Canneviè lagoon (Northern Adriatic Sea, Italy) was obtained from local fishermen. The fish were examined for the presence of endoparasitic helminths. Twenty-six eels (67%) harbored third-stage larvae (L3) of Contracaecum rudolphii A and the intensity of infection ranged from 1 to 100 parasites per fish (mean 11.4). A total of 296 larvae were counted and 293 were alive and encysted in the serosa (primarily on external surface of the rectum) as conspicuous granulomas, appearing as white nodules. Histological sections showed a granuloma formed around an individual larva and consisted of three concentric cell layers, containing numerous mast cells (MCs), fibroblasts, macrophages, and epithelioid cells. Encysted larvae were also present in other layers of the intestinal wall, including the mucosa, where recruitment of macrophage aggregates in lamina propria was documented. Immunohistochemical investigations, applying eight antibodies raised against immune cell markers, revealed histamine and serotonin in MCs and inducible-nitric oxide synthase and toll-like receptor-2 in macrophages surrounding the parasite larvae. The study indicates that this innate cellular response in the eel has a chronic inflammatory character and keeps the nematode larvae arrested in a state allowing both host tolerance and parasite survival. The European eel serves as prey for birds and the high survival of C. rudolphii A larvae in the eel indicates that this fish species is a good paratenic host for the parasite allowing completion of its life cycle in birds.