Anguillicola crassus (Nematoda, Dracunculoidea) infections of European eel (Anguila anguilla) in the Netherlands : epidemiology, pathogenensis and pathobiology

Research output: Thesisexternal PhD, WU


In the 1980s an eel parasitic nematode, Anguillicola crassus (Nematoda, Dracunculoidea), which infects the swimbladder of European eels ( Anguilla anguilla ) and other freshwater fish species, was introduced into The Netherlands. This thesis describes the epidemiology, pathogenesis, and pathobiology of the parasitic infection.

Originating from Southeast Asia, the parasite caused severe swimbladder lesions in European eels soon after its introduction: dilation of blood vessels, inflammation and rupture of the swimbladder in both wild and farmed eels, often resulting in severe fibrosis of the swimbladder ( chapter 2 ). High prevalences of infection were recorded (80 to 100% in 1987 in Dutch inland waters). Elvers became infected directly after entering the freshwater. Furthermore, the parasite was able to reach adulthood in the swimbladder lumen of these small eels. Infected farmed eels were particularly susceptible to secondary bacterial infections, which caused additional mortalities.

When fish from Dutch lakes were subsequently investigated for A. crassus ( chapter 3 ), it was found that freshwater smelt ( Osmerus eperlanus ), ruffe ( Gymnocephalus cernuus ), perch ( Perca fluviatilis ), zander ( Stizostedion lucioperca ), and three-spined stickleback ( Gasterosteus aculeatus ) contained third stage (L3) larvae of A. crassus in their swimbladders. Roach ( Rutilus rutilus ) and bream ( Abramis brama ), however, did not contain the nematode. Pro-adult A. crassus were also found in ruffe, perch, and three- spined stickleback, but adult specimens were missing. It was suggested, that some of the fish species containing L3 larvae are preyed upon by eels and may act as paratenic hosts for the transmission of the parasite to eels.

To test whether L3 larvae of A. crassus could be transmitted from infected smelt and ruffe to uninfected eels, eels were force-fed with infected smelt or ruffe swimbladders ( chapter 4 ). The L3 larvae migrated actively to the eel swimbladders, where they developed into adult A. crassus . It was concluded that eels can indeed become infected by eating infected prey fish.

In experimentally induced infections using oral inoculation of L3 larvae, the pathogenesis of A. crassus infection was studied ( chapter 5 ). L3 larvae migrated directly through the intestinal wall and body cavity of the eels to the swimbladder within only 17 h. Fourth-stage A. crassus larvae were detected 3 months after infection, and pre-adults within 4 months after infection. The L3 larvae occasionally showed aberrant migration paths. The lesions of the swimbladders were less severe than those of naturally infected eels. A. crassus developed much faster in the European eels than in the Japanese eel, Anguilla japonica , as reported in the literature.

The pathobiology of A. crassus in The Netherlands was investigated from 1986 to 1992 in freshwater eels and smelts ( chapter 6 ). Throughout the 6-year sampling period, young eels (up to 17 cm) showed severe lesions due to the parasite. Larger eels (23-34 cm) showed the highest prevalence of infection (96% from 1987 to 1988) and the highest intensity of infection, defined as the number of parasites per Infected fish (about 16 per fish from 1988 to 1989). After 1989 the prevalence and the severity of the swimbladder lesions decreased. Although larger eels (23-34 cm) from the Waddenzee (salt water) showed high prevalences of infection (85-90%) from 1987 to 1990, the intensities of infection decreased (7.7 to 4.8 per eel) from 1987 onwards, and the percentage of fibrotic swimbladders decreased from 1988 (maximum 24.5%). Smelts showed a sharp decrease in prevalence (88% to 48%) of the parasite shortly after 1988. Thereafter the prevalence stayed rather constant, at about 40% of the smelt population. No pathological changes were observed in the smelt.

By improving our method for producing infective L3 larvae of A. crassus , we were able to isolate distinct L3 larvae from copepods (intermediate host) and to count exactly the infective L3 larvae for inoculating eels ( chapter 7 ). This method was used in subsequent experiments.

To investigate why the A. crassus infection in naturally infected eels began to decrease, we conducted a dose-effect experiment in which some eels were primed and others not ( chapter 8 ). At day 0 uninfected eels were orally infected with various doses up to 40 L3 larvae of A. crassus per fish. At day 56 eels were either killed and examined, or were reinfected with 20 larvae each. At day 112 all remaining eels were killed and examined. The numbers of A. crassus recovered from the eels ranged between 14-20% at day 56 and 9-26% at day 112. These percentages were positively related to the total infection dose. There was no difference in percentages between primary and secondary infection. The swimbladder lesions were also positively related to the total dose, but were again not related to reinfection.

An enzyme linked immuno sorbent assay (ELISA) was developed to test blood samples for antibodies against adult cuticula antigen of A. crassus ( chapter 8 ). None of the sera from the experimental eels showed a titer in the ELISA, whereas sera from naturally infected eels showed high titers. However, when these sera were tested in Western blots, no protein band indicating specific antibodies against A. crassus cuticula antigen was detected. It was concluded that under our experimental conditions, the eels do not develop an antibody response or resistance against the parasite. Future research should focus on examining the possible roles of specific and nonspecific immune responses in the decrease in the A. crassus infection in naturally infected eels.

Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • van Muiswinkel, W.B., Promotor, External person
  • Borgsteede, F.H.M., Promotor
Award date10 Mar 1995
Place of PublicationWageningen
Print ISBNs9789054853541
Publication statusPublished - 1995


  • pests
  • animal diseases
  • animal pathology
  • anguillidae
  • eels
  • nematoda
  • parasites
  • fish stocks


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