Proliferative kidney disease: cellular aspects of the rainbow trout, Oncorhynchus mykiss (Walbaum), response to parasitic infection

Proliferative kidney disease (PKD) is an immunopathological condition of salmonid fish, caused by the hyperplastic response of their principal lymphoid tissues to infection with the spores of Tetracapsula bryosalmonae , a myxozoan parasite formerly designated proliferative kidney organism – unknown (PKX). In order to investigate the nature of cells involved in this host response and possible alterations of their functions during parasitic infection the course of PKD was studied by flow cytometry (FCM) techniques, using blood, pronephros and spleen leucocyte populations from rainbow trout infected by intraperitoneal (i.p.) injection with parasitic cells from infected donor fish. The parameters of the cellullar response studied were: cytogram of cell population, lymphoproliferation, phagocytosis, oxidative burst, and non-specific cytotoxicity. The modifications of cell population distribution and function in the PKD-infected fish mainly affected the pronephros cell populations and were coincident with the clinical phase of disease. During this phase, the lymphocytes constituted the major leucocyte cell population and underwent proliferation and were thus responsible for the renal tissue hyperplasia. Meanwhile, phagocytosis and oxidative burst were depressed. These data are in agreement with the patho-epidemiological background of PKD where the enhancement of the fish sensitivity to bacterial infections reflects the impairment of certain cellular defence mechanisms of innate immunity.     

Proliferative kidney disease and renal myxosporidiosis in juvenile salmonids from rivers in England and Wales

The results from a survey for proliferative kidney disease (PKD) and renal myxosporidiosis in wild salmonids from rivers in England and Wales are presented. One hundred and eighty-five salmon, Salmo salar , 235 brown trout, Salmo trutta , 16 charr, Salvelinus alpinus, and five grayling, Thymallus thymallus, were obtained from 23 locations on 16 rivers between July and October 1997. They were examined for the presence of clinical PKD and for histological evidence of infections with Tetracapsula bryosalmonae and other renal myxozoans. Prevalence of infection with T. bryosalmonae detected histologically in brown trout varied from 11 to 43% in enzootic rivers and was only found in salmon in two rivers at low prevalence. Nephromegaly was positively associated with PKD in brown trout but in salmon mild nephromegaly was only associated with infection with an unidentified Chloromyxum sp.     

Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans

The initial site of infection in the fish host for Tetracapsula bryosalmonae , causative agent of proliferative kidney disease (PKD) is poorly understood. Following the recent recognition that freshwater bryozoans harbour the infective stages to salmonid fish, experimental transmission studies were undertaken to investigate (1) the route of entry of the parasite into the fish host and (2) the minimum exposure time required to induce clinical signs of PKD. In-situ hybridization (ISH) studies were carried out on naïve rainbow trout exposed to the naturally infected bryozoan Fredericella sultana for up to 90 min. The sporoplasm of T. bryosalmonae was detected entering the fish via mucous cells in the skin epithelium within the first minute of exposure. In addition, T. bryosalmonae cells were infrequently detected in the skeletal musculature of exposed experimental fish up to 72 h post-exposure. The route of migration through the fish to the kidney and spleen was not determined. All fish exposed to infected, disrupted bryozoans for 10, 30 and 90 min and maintained for up to 8 weeks developed clinical PKD.     

An understated danger: Antimicrobial resistance in aquaculture and pet fish in Switzerland,a retrospective study from 2000 to 2017

Aquaculture is a rapidly growing field of food production. However, morbidity and mortality are higher in aquaculture species than in domestic animals. Bacterial diseases are a leading cause of farmed fish morbidity and are often treated with antimicrobials. Since most Swiss fish farms release effluents directly into surface water without treatment and since aquaculture fish are consumed by humans, antimicrobial resistance (AMR) and multi-resistance in aquaculture fish are important for environmental and public health. In this study, AMR tests for 14 antimicrobials were performed on 1,448 isolates from 1,134 diagnostic laboratory submissions from farmed and ornamental fish submissions for the period from 2000 to 2017. Amoxicillin, gentamycin and norfloxacin had the lowest proportion of resistant samples. However, AMR was highly variable over time. Resistance proportions were higher in: (a) ornamental fish compared with farmed fish, (b) fish from recirculation systems compared with those from other farming systems and (c) isolates originating from skin compared with those originating from inner organs. Multiple resistances were common. The results of this study provide useful data for Swiss fish veterinarians and some interesting hypotheses about risk factors for AMR in aquaculture and pet fish in Switzerland. However, further research is needed to define risk factors.     

A brown trout (Salmo trutta) population faces devastating consequences due to proliferative kidney disease and temperature increase: A case study from Austria

Proliferative kidney disease (PKD) is an emerging parasitic disease that affects wild and farmed salmonid fishes worldwide. Currently, it is widespread in Europe with records in many countries. This study assessed the status of PKD in the river Wulka, a small Austrian river, which was known to host a vital brown trout population despite having high water temperatures. Contrary to the initial hypothesis that the river was free from PKD, we observed an overall PKD prevalence of 92%. Noninfected fish were restricted to the uppermost river section. Twenty-two out of 87 PKD-positive fish of all age classes showed clinical signs, while five individuals exhibited signs of recovering from PKD infection. The severity of clinical signs was significantly dependent on the fish length and age, with smaller or younger individuals being more severely affected. Comparison of data from the earlier fish sampling events with those results from 2017 and 2018, together with the analyses of the pattern of water temperature since 2010, indicates that Wulka's brown trout population might become extinct in the near future.     

A survey of viral diseases in farmed and feral salmonids in Switzerland

A field survey was carried out to study the occurrence and distribution of viruses causing diseases of major impact in fish farming, namely viral haemorrhagic septicaemia (VHS), infectious haematopoietic necrosis (IHN) and infectious pancreatic necrosis (IPN) in farmed and wild fish in Switzerland. The presence of VHS virus (VHSV), IHN virus (IHNV) and IPN virus (IPNV) in the tissue samples was tested by virus isolation in cell cultures, and subsequent virus identification by immunofluorescence. The sera were screened for anti-VHSV antibodies (VHSV-AB) using a serum plaque neutralization test with complement addition. These data were then compared with results of a similar survey performed in 1984/85, and with data from routine diagnostic work completed at the Centre for Fish and Wildlife Health (FIWI) of the University of Bern from 1978 to 2001. Sampling sites included private and government fish farms as well as natural habitats from all major river catchments in Switzerland. In 2000/01, 522 tissue samples and 1910 sera were collected from 3400 fish. In 1984/85 1239 tissue samples and 694 sera were collected from 1628 fish. During the last 24 years of routine diagnostics at the FIWI, 1776 tissue samples were examined for presence of viruses. The results of the tissue analysis from the surveys in 1984/85 and 2000/01 showed low numbers of sites with virus-positive fish (five VHSV, three IPNV and three VHSV, one IPNV, respectively) in Swiss fish farms and rivers. The sites with virus-positive fish were located throughout the country. The decline in virus-positive cases observed between the two surveys agrees with data from the routine diagnostic work of the FIWI which show a decrease in total virus isolations from approximately 35 cases per year in the late 1970s, to approximately 10 cases per year during the last 10 years. However, in 1984/85 8.3% (58 of 694 serum samples) and in 2000/01 6.3% (121 of 1910 serum samples) proved to be positive for VHSV-AB. The 58 positive samples in 1984/85 originated from 40 of 175 sites (23%) and the 121 positive samples in 2000/01 were from 84 of 217 (29%) sites. These results are indicative of a wider distribution of VHSV than expected from the results of the virus isolations.     

Patterns of Tetracapsuloides bryosalmonae infection of three salmonid species in large,deep Norwegian lakes

Proliferative kidney disease (PKD), caused by the myxozoan endoparasite Tetracapsuloides bryosalmonae, is of serious ecological and economical concern to wild and farmed salmonids. Wild salmonid populations have declined due to PKD, primarily in rivers, in Europe and North America. Deep lakes are also important habitats for salmonids, and this work aimed to investigate parasite presence in five deep Norwegian lakes. Kidney samples from three salmonid species from deep lakes were collected and tested using real-time PCR to detect PKD parasite presence. We present the first detection of T. bryosalmonae in European whitefish in Norway for the first time, as well as the first published documentation of the parasite in kidneys of Arctic charr, brown trout and whitefish in four lakes. The observed prevalence of the parasite was higher in populations of brown trout than of Arctic charr and whitefish. The parasite was detected in farmed, but not in wild, charr in one lake. This suggests a possible link with a depth of fish habitat and fewer T. bryosalmonae-infected and PKD-affected fish. Towards a warmer climate, cold hypolimnion in deep lakes may act as a refuge for wild salmonids, while cold deep water may be used to control PKD in farmed salmonids.     

Modeling optimal dietary pigmentation strategies in farmed Atlantic salmon: Application of mixed-integer non-linear mathematical programming techniques

The most important visual quality characteristic of Atlantic salmon is the red/pink flesh color. The primary source of this coloration in salmon is caused by deposition of relatively large amounts of pigments, such as astaxanthin, obtained from their diet. Astaxanthin is expensive, and in commercial farming practice, dietary color pigments comprises about 15-20% of the total feed cost. One important operational process in commercial fish farms is therefore to minimize pigment costs. Based on recent models on the effects of dietary pigment concentration and fish size on visual color perception of Atlantic salmon, this study has built a mathematical programming model designed to optimize dietary astaxanthin concentrations throughout the grow-out period that results in well-pigmented fish at minimum cost. We have applied a mixed-integer non-linear programming algorithm to solve this problem. Various managerial implications of applying optimization models in product quality management of farmed salmon are discussed.     

Diagnosis of bacterial kidney disease by detection of Renibacterium salmoninarum by real-time PCR

Bacterial kidney disease (BKD), caused by Renibacterium salmoninarum (Rs), is a serious threat to salmon in aquaculture as well as to wild populations. We have developed a real-time polymerase chain reaction (PCR) for detection of Rs in kidney samples. The PCR is based on detection of unique parts of the 16S rRNA gene of Rs and DNA equivalent to 1-10 Rs genomes was detected per reaction. No cross-reactivity with other fish pathogenic or related bacteria could be demonstrated. Analysis of individual kidney samples collected from BKD classified populations identified 39.9% of the fish as positive by real-time PCR compared with 28.0% by polyclonal enzyme-linked immunosorbent assay (ELISA). The real-time PCR assay was found to be well suited for complementary use with ELISA for diagnosis of BKD, with the ability to detect clinical as well as covert Rs infections. The infection level determined by the polyclonal ELISA and by real-time PCR was significantly correlated.     

Randomized clinical field trial of a bacterial kidney disease vaccine in Atlantic salmon,Salmo salar L.

A randomized, blinded clinical trial was performed to assess the relative effectiveness of five commercial and one experimental vaccine in a population of farmed fish experiencing a bacterial kidney disease (BKD) outbreak that occurred in one study cage that was part of a larger clinical field trial. A total of 6000 uniquely identified Atlantic salmon S1 presmolts were randomly assigned to vaccine groups in the hatchery and transferred to a commercial marine aquaculture site. Repeated sampling events to evaluate growth, inherent physical conditions and health status were carried out over the entire production cycle. During the second summer at sea, the study cage developed an outbreak of BKD that lasted approximately 240 days. The effectiveness of the selected vaccines was evaluated using survival analysis methods. The sole vaccine group offering protection for BKD was found to significantly decrease the hazard of dying (hazard ratio, HR = 0.68, P = 0.018) during the outbreak, compared to the industry standard, vaccine group. Additionally, during the outbreak, fish with a shortened operculum had a significantly decreased hazard (HR = 0.38, P = 0.033) compared to those fish with a normal operculum, while fish with jaw deformities had a significantly increased hazard (HR = 2.55, P = 0.001) compared to fish with normal jaw status.     

Cardiomyopathy syndrome in Atlantic salmon Salmo salar L.: A review of the current state of knowledge

Cardiomyopathy syndrome (CMS) is a severe cardiac disease affecting Atlantic salmon Salmo salar L. The disease was first recognized in farmed Atlantic salmon in Norway in 1985 and subsequently in farmed salmon in the Faroe Islands, Scotland and Ireland. CMS has also been described in wild Atlantic salmon in Norway. The demonstration of CMS as a transmissible disease in 2009, and the subsequent detection and initial characterization of piscine myocarditis virus (PMCV) in 2010 and 2011 were significant discoveries that gave new impetus to the CMS research. In Norway, CMS usually causes mortality in large salmon in ongrowing and broodfish farms, resulting in reduced fish welfare, significant management‐related challenges and substantial economic losses. The disease thus has a significant impact on the Atlantic salmon farming industry. There is a need to gain further basic knowledge about the virus, the disease and its epidemiology, but also applied knowledge from the industry to enable the generation and implementation of effective prevention and control measures. This review summarizes the currently available, scientific information on CMS and PMCV with special focus on epidemiology and factors influencing the development of CMS.     

Proliferative kidney disease (PKD) in rainbow trout Salmo gairdneri: Further observations on the effects of water temperature

The seasonality of proliferative kidney disease (PKD) and the effects of water temperature on the development of the disease in naturally-infected fingerling rainbow trout, Salmo gairdneri, were investigated. Fingerling rainbow trout became infected from May to October, but those infected in October did not develop clinical disease. In naturally-infected fish subsequently held under laboratory conditions, clinical PKD occurred at 12–18°C, but not at 9°C. The disease progressed more rapidly and was more severe as temperatures increased. On re-exposure to infection, rainbow trout previously held at 9°C developed clinical PKD, whereas in those previously held at 12°C it did not develop. Possible implications of these findings for the control of PKD are discussed.     

Distribution and prevalence of T. bryosalmonae in Austria: A first survey of trout from rivers with a shrinking population

The first evidence of proliferative kidney disease (PKD) in an Austrian river (the River Kamp) was documented in 2016, and no information on the PKD infection status of trout in other rivers was available. Since then, brown trout (Salmo trutta fario) and rainbow trout (Oncorhynchus mykiss) have been collected from rivers in Upper and Lower Austria for different diagnostic purposes. In this study, we summarize the recent findings of a first survey concerning the distribution of Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD), from these samples. Between September 2015 and October 2017, a total of 280 brown trout and 39 rainbow trout were collected from 21 rivers in the provinces of Upper and Lower Austria. T. bryosalmonae was detected by PCR of kidney tissue in 17 of 21 sampled rivers and in 138 of 280 brown trout as well as in 11 of 39 rainbow trout. Pathological signs of PKD (e.g., hypertrophy of the kidney) were observed in 33 analysed brown trout and six rainbow trout samples. No correlations between fish infected by T. bryosalmonae and the parameters size and age class, condition factor, geological origin of the streams and distribution within the river course were found, while positively tested fish are significantly increased at sampling sites exceeding water temperatures of 15°C for median periods of 115 days. The prevalence within the affected streams or stream sections is highly variable, and in single rivers, infection rates of up to 90% are confirmed.     

Systematic point sampling of fish communities in medium‐ and large‐sized rivers: sampling procedure and effort

Compared with small rivers and streams, the study of fish communities in large rivers remains challenging as spatial and temporal data variability can be greatly influenced by sampling strategy and operator choice. In an attempt to limit this variability, a new sampling protocol for fish communities in medium‐ to large‐sized rivers was developed, based on point sampling by electric fishing and using standardised procedures and effort. Here, change in data quality (assemblage abundance, richness, structure and biotic index) with increasing sampling effort (from 1 to 100 sampling points) was evaluated. A total of 75 sampling points are proposed as the standard number of samples per site. Broadly, the results show that the application of 75 sampling points provides a reproducible representation of fish community structure in medium and large rivers, with little additional information provided by further sampling except under certain conditions, when 100 points are recommended to maintain data quality.