PERSISTENCE OF THE VIRULENCE OF AEROMONAS SALMONICIDA STRAINS KEPT IN RIVER SEDIMENTS
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1 PERSISTENCE OF THE VIRULENCE OF AEROMONAS SALMONICIDA STRAINS KEPT IN RIVER SEDIMENTS C. MICHEL Annie DUBOIS-DARNAUDPEYS 2 Laboratoire d /chtyopatho%gie, l.n.r.a., Thiverval-Grignon, France. 2 Laboratoire Central de Recherches Vétérinaires, Direction de la Qualité, Maisons-Alfort cedex, France. Résumé PERSISTANCE DU POUVOIR PATHOGÈNE D AEROMONAS SALMONlClDA APRÈS CON- SERVATION DANS LA VASE DE RIVIÈRE. ― La persistance du pouvoir pathogène de deux souches d Aeromonas salmonicida a été étudiée lors de leur entretien dans la vase de rivière. Les cultures ont été gardées environ neuf mois, la virulence faisant l objet de comparaisons avec celle des mêmes souches, entretenues sur truitelles arc-en-ciel. Pour ce, des doses comparables de bactéries étaient injectées par voie intramusculaire à des lots de 30 poissons élevés à 15 C, et les mortalités résultantes étaient enregistrées. Aucune différence n a pu être décelée au cours des six premiers mois, après quoi la virulence s est atténuée jusqu à disparaître avant le neuvième mois. Les températures d incubation ont également été abaissées par paliers, afin de simuler les conditions d hivernage, sans que le devenir du pouvoir pathogène s en trouve altéré. Le rôle potentiel de la vase comme source d infection pour les poissons est discuté. Aeromonas salmonicida has been frequently isolated from salmonid and non-salmonid fish displaying no sign of furunculosis, but up to now, little was known of its persistence in the environment. Experimental work, conducted at the beginning of the century demonstrated the active multiplication of the germ in sewage and polluted water (Plehn, 1924 ; Duff et al., 1940) in contrast with its poor ability to survive in non-polluted water (Mc Craw, 1952). In 1962 Smith obtained a survival of three weeks in a simulated rock bottom. Similar results were recently reported by observing the A. sa/- monicida multiplication on aquatic plants and in sediments (Dubois-Darnaudpeys, 1977a). Moreover, the regular detection of specific phages in mud samples of a river was an indirect demonstration of the presence of the bacteria all through the year (Dubois- Darnaudpeys, 1977c). Despite the fact that most of the authors have considered the germ as an obligatory pathogen exclusively disseminated by ill and carrier fish (Snieszko, 1972 ; Wolke, 1975 ; Richards and Roberts, 1978), such an observation raises the question of a possible role of the environment in the disease transmission. However, before attributing some credibility to this contingency, it was necessary to verify that the pathogenic properties of A. salmonicida were not modified during its passage in mud, as often happens when it is subcultivated in artificial media.
2 Materials and Methods Bacterial strains Two virulent strains of A. salmonicida isolated at Thiverval-Grignon (TG 36/75 and TG 72/78) were used in experiments. Both were strongly self-aggregating and initially exhibited lethal doses 50 (LD 50) of about 1000 bacteria when injected intramuscularly (IM) to 7 g rainbow trout fingerlings. Maintenance in mud Flasks of 2 1 containing river mud were prepared according to a previously described technique (Dubois-Darnaudpeys, 1977a). Mud was sampled from the River Juine (Essonne), diluted in water at 1/4 (W/V) and sterilized at 135 C for 35 min. Inoculations were done with freshly isolated cultures from kidneys of experimentally infected trout. The incubation temperature was 15 C, but three flasks were submitted to thermal variations in order to simulate wintering conditions. Figure 1 expresses the different treatments applied to the cultures during the experiments. The dates on which samples were taken for checking the virulence of the bacteria were also recorded. Maintenance in trout In order to maintain the virulence at its highest degree and to dispose of convenient controls, the strains were simultaneously subcultivated in rainbow trout (Salmo gairdneril. Animals were injected every week via IM route with 0.1 ml of an infected fish kidney suspen-.sion. Dead fish were frozen at - 30 C as a source of virulent bacteria. They could be stored for about two months in such conditions before disappearance of the germ. Checking of virulence Rainbow trout also served to test the virulence of our strains. Their size ranged between 5 to 14 g according to the season. All experiments were done in 12 1 aquaria supplied with 15 C dechlorinated tap water and stocked with 30 fingerlings. Strains were periodically recovered from mud flasks and from kidneys of diseased fish, isolated on trypticase-soy-agar (TSA) and grown in tryptic soy broth (TSB) at 22 C for 24 hours. Cultures were stirred only for the 72/78 strain, for which a standardized model of production was available. Bacteria were yielded, and the suspensions which originated from mud and
3 kidneys were as much as possible adjusted at similar turbidities and diluted to a convenient dose for IM injection to fish. Controls were done by plate numeration technique, and anesthetized fish (MS 222 Sandoz) were inoculated. Mock infected controls received only 0.1 ml of saline at 6 g/i. Mortalities were recorded for a period of 10 days, and bacteriological examination of fish was performed. With the 72/78 strain a standard model of infection (Michel, 1980) allowed to obtain correct adjustement of doses and to compare directly the losses in the different aquaria. Although we were obliged to apply the Yates correction, chi-square tests could be employed without difficulty. It was not the case with 36/75, which was studied first, and for which we had to establish mortality curves and compare them to a reference curve previously observed, taking into account the variation in injected doses, which were poorly controlled. Results Strain TG 36/75 Four assessments of pathogenicity were carried out between the second and the tenth months, and the cumulative mortalities curves obtained both with bacteria maintained in mud and in trout are shown in figure 2. Bacteria were submitted to a decrease in temperature, but unfortunately the control kept at 15 C was lost, due to a Pseudomonas species contamination. From the third assay onward the virulence could no longer be observed with the bacteria isolated from mud. Strain TG 72/78 Three experiments were done, respectively after three, six and nine months of conservation. Except in the third, the mortalities were lower than expected, as seen in table 1, but no difference was found before the ninth month, when both the germs maintained at 15 C and
4 those submitted to a transitory passage at 8 C became avirulent. It must be noted that a flask exposed at 8 C was also contaminated before the last control and that A. salmonicida could not be reisolated. Discussion The two first evaluations of figure 2 resulted in mortality curves which do not differ markedly from the initial control curve. The fluctuations of injected doses of germs were caused by a lethal phenomenon occurring in nonstirred cultures and impairing the accurate adjustment of titers by the turbidimetric method. After the eighth month, bacteria isolated from mud were unable to kill any fish, even when large doses (up to 4 LD 50) were administered. As the strain had been submitted to a six months passage at 8 C, and as the cells maintained at 15 C had been lost, it was impossible to draw any conclusion concerning the cause of inactivation of the virulence. It might have been due both to the simulated wintering conditions and to the age of the culture. Confirmatory observations were done with the strain 72/78. Whatever the thermic exposition of the cultures, the virulence was well conserved for six months but disappeared before the ninth month. It seems therefore that temperature does not play a major role in the evolution of the pathogenic properties of A. salmonicida during its passage in mud. The low values of the mortality rates in the first and second checking up have been stressed. A technical fault was probably done in the first case, and doses lower than expected were injected to fish. When the second trial was carried out, in autumn, available trout were of different size and origin than those usually tested and proved more resistant to furunculosis. Nevertheless, it was possible to perform statistical analysis, applying the Yates correction to the 2x test. In the course of the study two flasks became contaminated with bacterial species related to the family of Pseudomonadaceae.
5 During the resulting competitive situation A. salmonicida was eliminated in less than one month and irreparably lost. This was to be expected, since an inhibitory effect for the pathogen had been described in mixed cultures with other microorganisms found in sediments. This effect was attributed to a production of bacteriocins (Dubois-Darnaudpeys, 1977b1. It appears from our experiments that the furunculosis agent is able to survive and grow in sterilized river sediments during a long time without noticeable decrease of its pathogenicity which persists for at least six months. In natural conditions such a duration would provide to the pathogen strong chances of being released in water, especially if burrowing animals belong to the biocoenosis of the stream, and to reach receptive species of fish living downstream. The habits of certain species, used to feeding on the bottom, also enable a direct contamination of fish, so attaining carrier status. It could be objected, and our own methodological difficulties support this view, that the presence in streams of large numbers of bacteria having a marked ability to synthesize bacteriocins may act as a regulatory mechanism and limit the proliferation of the germ. But previous work (Dubois-Darnaudpeys, 1977c) has been emphasized, which seems to substantiate a real persistence of A. salmonicida in certain natural sediments, and it is difficult to rule out the potential hazard of fish contamination from mud in furunculosis epidemiology, even though the direct contact with infected animals is likely to remain the main way of transmission. Acknowledgements This work was supported by the «Conseil Supérieur de la P6che», grants nos and Accepted for publication October 28th, 1,5180. Summary The persistence of pathogenicity in two strains of Aeromonas salmonicida maintained in river sediments was studied at different times. Cultures were kept about nine months, and the virulence was compared to its initial value exhibited by the same strains, subcultivated in rainbow trout fingerlings. Trials involved intramuscular injection of comparable doses of bacteria to batches of 30 fish held at 15 C, and recording of subsequent mortalities. No difference was found during the first six months, after which a decrease of the pathogenicity resulted in its disappearance before the ninth month. Progressive decrease in incubation temperatures was also exerted to simulate an artificial wintering, but did not alter the evolution of the virulence. The possible role of mud as a source of contamination for fish is discussed. References DUBOIS-DARNAUDPEYS A., 1977a.!pid6miologie de la furonculose des salmonid6s. I. Etude expérimentale des conditions de survie de Aeromonas salmonicida dans un environnement abiotique. Bull. Fr. Piscic., 49 (2C>4), DUBOIS-DARNAUDPEYS A., 1977b. Epid6miologie de la furonculose des salmonid6s. 11. Etude exp6rimentale de divers facteurs microbiotiques de 1 environnement. Bull. Fr. Piscic., 49 (265), DUBOIS-DARNAUDPEYS A., 1977c.!pid6miologie de la furonculose des salmonidés. 111.!cologie de Aeromonas salmonicida. Proposition d un modèle épidémiologique. Bull. Fr. Piscic., 50 (266), DUFF D.C.B., Mc ARTHUR M.T., THOMPSON H.G., Observations on viability of Bacterium salmonicida. J. Fish. Res. Board Can., 5, 1-7. Mc CRAW B.M., Furunculosis of fish, U.S. Dept. Interior, Fish and Wildlife Service, Sp. Sc. report : fisheries, no 84, 87 pp. MICHEL C., A standardized model of experimental furunculosis in rainbow trout (Salmo gairdneril. Can. J. Fish. Aquat. Sci., 37, PLEHN M., Praktikum der Fischkrankheiten. Schweizerbart, Stuttgart.
6 RICHARDS R.H., ROBERTS R.J., The bacteriology of Teleosts in ROBERTS R.J., Fish pathology, Baiiii6re-Tindal, London. SMITH I.W., Furunculosis in kelts. Department of Agriculture and Fisheries for Scotland, Freshwater and Salmon Fisheries Res., no 27, 12 pp. SNIESZKO S.F., Panel review on furunculosis of Salmonidae. FAO/EIFA, symposium on major communicable fish diseases in Europe and their control. Amsterdam. WOLKE R.E., Pathology of bacterial and fungal diseases affecting fish. in Ribelin W.E., and Migaki G., The patho%gy of fishes, University of Wisconsin Press, Madison, Wisconsin,
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