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Rachel Breyta

Publications and source records attributed to Rachel Breyta.

13 recordsLinked to original sources

Coproduction and modeling spatial contact networks prevent bias about infectious hematopoietic necrosis virus transmission for Snake River Basin salmonids

Much remains unknown about variation in pathogen transmission across the geographic range of a free-ranging fish or animal species and about the influence of movement (associated with husbandry practices or animal behavior) on pathogen transmission. Salmonid hatcheries are an ideal system in which to study these processes. Salmonid hatcheries are managed for endangered species recovery, supplementation of threatened or at-risk fish stocks, support of fisheries, and ecosystem stability. Infectious hematopoietic necrosis virus (IHNV) is a rhabdovirus of significant concern to salmon aquaculture. Landscape IHNV transmission dynamics previously had been estimated only for salmonid hatcheries in the Lower Columbia River Basin (LCRB). The objectives of this study were to estimate IHNV transmission dynamics in a unique geographic region, the Snake River Basin (SRB), and to quantitatively estimate the effect of model coproduction on inference because previous assessments of coproduction have been qualitative. In contrast to the LCRB, the SRB has hatchery complexes consisting of a main hatchery and ≥1 satellite facility. Knowledge about hatchery complexes was held by a subset of project researchers but would not have been available to project modelers without coproduction. Project modelers generated and tested multiple versions of Bayesian susceptible-exposedinfected models to realistically represent the SRB and estimate the effect of coproduction. Models estimated the frequency of transmission routes, route-specific infection probabilities, and infection probabilities for combinations of salmonid hosts and IHNV lineages. Model results indicated that in the SRB, avoiding exposure to IHNV-positive adult salmonids is the most important action to prevent juvenile infections. Migrating adult salmonids exposed juvenile cohort-sites most frequently, and the infection probability was greatest following exposure to migrating adults. Without coproduction, the frequency of exposure by migrating adults would have been overestimated by 70 cohort-sites, and the infection probability following exposure to migrating adults would have been underestimated by∼0.09. The coproduced model had less uncertainty in the infection probability if no transmission route could be identified (Bayesian credible interval (BCI) width = 0.12) compared to the model without coproduction (BCI width = 0.34). Evidence for virus lineage MD specialization on steelhead and rainbow trout (both Oncorhynchus mykiss) was apparent without model coproduction. In the SRB, we found a greater probability of virus lineage UC infection in Chinook salmon (Oncorhynchus tshawytscha) compared to in O. mykiss, whereas in the LCRB, UC more clearly exhibited a generalist approach. Coproduction influenced estimates that depended on transmission routes, which operated differently at main hatcheries and satellite sites within hatchery complexes. Hatchery complexes are found outside of the SRB and are not specific to salmonid hatcheries alone. There is great potential for coproduction and modeling spatial contact networks to advance understanding about infectious disease transmission in complex production systems and surrounding free-ranging animal populations.

Idaho, Oregon, Washington

Genetics reveal long-distance virus transmission links in Pacific salmon

In the coastal region of Washington State, a major pathogen emergence event occurred between 2007 and 2011 in which steelhead trout ( Oncorhynchus mykiss ) experienced a high incidence of infection and disease outbreaks due to the rhabdovirus infectious hematopoietic necrosis virus (IHNV). Genetic typing showed that the introduced viruses were in the steelhead-specific MD subgroup of IHNV and indicated the most likely source was a virus from the nearby Columbia River Basin. In the current study, full-length viral glycoprotein (G) gene sequences were determined for 55 IHNV isolates from both coastal and Columbia fish populations to identify specific source populations and infer mechanisms of transmission to coastal steelhead. We identified three transmission links based on exact fullG genotype matches between Columbia and coastal fish. In all cases, the likely source population was infected juvenile fish, and sink populations were adult fish returning to coastal rivers to spawn. The time intervals between detection in source and sink populations varied from 6 months to nearly 4 years, suggesting different transmission pathways. Surprisingly, distances between source and sink populations varied between 140 and 1000 km. These results confirm repeated introductions of virus from Columbia River Basin fish as the cause of emergence of MD virus on the Washington coast from 2007 to 2011. View Full-Text

Washington

Rapid diagnostic test to detect and discriminate infectious hematopoietic necrosis virus (IHNV) genogroups U and M to aid management of Pacific Northwest salmonid populations

Infectious hematopoietic necrosis virus (IHNV) is an acute pathogen of salmonids in North America, Europe, and Asia that is phylogenetically classified into five major virus genogroups (U, M, L, E, and J). The geographic range of the U and M genogroup isolates overlap in the North American Columbia River Basin and Washington Coast region, where these genogroups pose different risks depending on the species of Pacific salmon ( Oncorhynchus spp.). For certain management decisions, there is a need to both test for IHNV presence and rapidly determine the genogroup. Herein, we report the development and validation of a U/M multiplex reverse transcription, real-time PCR (RT-rPCR) assay targeting the IHNV nucleocapsid (N) protein gene. The new U/M RT-rPCR is a rapid, sensitive, and repeatable assay capable of specifically discriminating between North American U and M genogroup IHNV isolates. However, one M genogroup isolate obtained from commercially cultured Idaho rainbow trout ( O. mykiss ) showed reduced sensitivity with the RT-rPCR test, suggesting caution may be warranted before applying RT-rPCR as the sole surveillance test in areas associated with the Idaho trout industry. The new U/M assay had high diagnostic sensitivity (DSe > 94%) and specificity (DSp > 97%) in free-ranging adult Pacific salmon, when assessed relative to cell culture, the widely accepted reference standard, as well as the previously validated universal N RT-rPCR test. The high diagnostic performance of the new U/M assay indicates the test is suitable for surveillance, diagnosis, and confirmation of IHNV in Pacific salmon from the Pacific Northwest regions where the U and M genogroups overlap.

Animals

Infectious hematopoietic necrosis virus specialization in a multihost salmonid system

Many pathogens interact and evolve in communities where more than one host species is present, yet our understanding of host–pathogen specialization is mostly informed by laboratory studies with single species. Managing diseases in the wild, however, requires understanding how host–pathogen specialization affects hosts in diverse communities. Juvenile salmonid mortality in hatcheries caused by infectious hematopoietic necrosis virus (IHNV) has important implications for salmonid conservation programs. Here, we evaluate evidence for IHNV specialization on three salmonid hosts and assess how this influences intra‐ and interspecific transmission in hatchery‐reared salmonids. We expect that while more generalist viral lineages should pose an equal risk of infection across host types, viral specialization will increase intraspecific transmission. We used Bayesian models and data from 24 hatcheries in the Columbia River Basin to reconstruct the exposure history of hatcheries with two IHNV lineages, MD and UC, allowing us to estimate the probability of juvenile infection with these lineages in three salmonid host types. Our results show that lineage MD is specialized on steelhead trout and perhaps rainbow trout (both Oncorhynchus mykiss ), whereas lineage UC displayed a generalist phenotype across steelhead trout, rainbow trout, and Chinook salmon. Furthermore, our results suggest the presence of specialist–generalist trade‐offs because, while lineage UC had moderate probabilities of infection across host types, lineage MD had a small probability of infection in its nonadapted host type, Chinook salmon. Thus, in addition to quantifying probabilities of infection of socially and economically important salmonid hosts with different IHNV lineages, our results provide insights into the trade‐offs that viral lineages incur in multihost communities. Our results suggest that knowledge of the specialist/generalist strategies of circulating viral lineages could be useful in salmonid conservation programs to control disease.

Oregon, Washington

An epidemiological model of virus transmission in salmonid fishes of the Columbia River Basin

We have developed a dynamic epidemiological model informed by records of viral presence and genotypes to evaluate potential transmission routes maintaining a viral pathogen in economically and culturally important anadromous fish populations. In the Columbia River Basin, infectious hematopoietic necrosis virus (IHNV) causes severe disease, predominantly in juvenile steelhead trout ( Oncorhynchus mykiss ) and less frequently in Chinook salmon ( O. tshawytscha ). Mortality events following IHNV infection can be devastating for individual hatchery programs. Despite reports of high local mortality and extensive surveillance efforts, there are questions about how viral transmission is maintained. Modeling this system offers important insights into disease transmission in natural aquatic systems, as well as about the data requirements for generating accurate estimates about transmission routes and infection probabilities. We simulated six scenarios in which testing rates and the relative importance of different transmission routes varied. The simulations demonstrated that the model accurately identified routes of transmission and inferred infection probabilities accurately when there was testing of all cohort-sites. When testing records were incomplete, the model accurately inferred which transmission routes exposed particular cohort-sites but generated biased infection probabilities given exposure. After validating the model and generating guidelines for result interpretation, we applied the model to data from 14 annual cohorts (2000–2013) at 24 focal sites in a sub-region of the Columbia River Basin, the lower Columbia River (LCR), to quantify the relative importance of potential transmission routes in this focal sub-region. We demonstrate that exposure to IHNV via the return migration of adult fish is an important route for maintaining IHNV in the LCR sub-region, and the probability of infection following this exposure was relatively high at 0.16. Although only 1% of cohort-sites experienced self-exposure by infected juvenile fish, this transmission route had the greatest probability of infection (0.22). Increased testing and/or determining whether transmission can occur from cohort-sites without testing records (e.g., determining there was no testing record because there were no fish at the cohort-site) are expected to improve inference about infection probabilities. Increased use of secure water supplies and continued use of biosecurity protocols may reduce IHNV transmission from adult fish and juvenile fish within the site, respectively, to juvenile salmonids at hatcheries. Models and conclusions from this study are potentially relevant to understanding the relative importance of transmission routes for other important aquatic pathogens in salmonids, including the agents of bacterial kidney disease and coldwater disease, and the basic approach may be useful for other pathogens and hosts in other geographic regions.

Ecological Modelling

Molecular systematics of sturgeon nucleocytoplasmic large DNA viruses

Namao virus (NV) is a sturgeon nucleocytoplasmic large DNA virus (sNCLDV) that can cause a lethal disease of the integumentary system in lake sturgeon Acipenser fulvescens . As a group, the sNCLDV have not been assigned to any currently recognized taxonomic family of viruses. In this study, a data set of NV DNA sequences was generated and assembled as two non-overlapping contigs of 306,448 bp and then used to conduct a comprehensive systematics analysis using Bayesian inference of phylogeny for NV, other sNCLDV and representative members of six families of the NCLDV superfamily. The phylogeny of NV was reconstructed using protein homologues encoded by nine nucleocytoplasmic virus orthologous genes (NCVOGs): NCVOG0022 – mcp, NCVOG0038 – DNA polymerase B elongation subunit, NCVOG0076 – VV A18-type helicase, NCVOG0249 – VV A32-type ATPase, NCVOG0262 – AL2 VLTF3-like transcription factor, NCVOG0271 – RNA polymerase II subunit II, NCVOG0274 – RNA polymerase II subunit I, NCVOG0276 – ribonucleotide reductase small subunit and NCVOG1117 – mRNA capping enzyme. The accuracy of our phylogenetic method was evaluated using a combination of Bayesian statistical analysis and congruence analysis. Stable tree topologies were obtained with data sets differing in target molecule(s), sequence length and taxa. Congruent topologies were obtained in phylogenies constructed using individual protein data sets. The major capsid protein phylogeny inferred that ten representative sNCLDV form a monophyletic group comprised of four lineages within a polyphyletic Mimi-Phycodnaviridae group of taxa. Overall, the analyses revealed that Namao virus is a member of the Mimiviridae family with strong and consistent support for a clade containing NV and CroV as sister taxa.

Molecular Phylogenetics and Evolution

Transmission routes maintaining a viral pathogen of steelhead trout within a complex multi-host assemblage

This is the first comprehensive region wide, spatially explicit epidemiologic analysis of surveillance data of the aquatic viral pathogen infectious hematopoietic necrosis virus (IHNV) infecting native salmonid fish. The pathogen has been documented in the freshwater ecosystem of the Pacific Northwest of North America since the 1950s, and the current report describes the disease ecology of IHNV during 2000–2012. Prevalence of IHNV infection in monitored salmonid host cohorts ranged from 8% to 30%, with the highest levels observed in juvenile steelhead trout. The spatial distribution of all IHNV-infected cohorts was concentrated in two sub-regions of the study area, where historic burden of the viral disease has been high. During the study period, prevalence levels fluctuated with a temporal peak in 2002. Virologic and genetic surveillance data were analyzed for evidence of three separate but not mutually exclusive transmission routes hypothesized to be maintaining IHNV in the freshwater ecosystem. Transmission between year classes of juvenile fish at individual sites (route 1) was supported at varying levels of certainty in 10%–55% of candidate cases, transmission between neighboring juvenile cohorts (route 2) was supported in 31%–78% of candidate cases, and transmission from adult fish returning to the same site as an infected juvenile cohort was supported in 26%–74% of candidate cases. The results of this study indicate that multiple specific transmission routes are acting to maintain IHNV in juvenile fish, providing concrete evidence that can be used to improve resource management. Furthermore, these results demonstrate that more sophisticated analysis of available spatio-temporal and genetic data is likely to yield greater insight in future studies.

Idaho, Oregon, Washington

Infectious hematopoietic necrosis virus virological and genetic surveillance 2000–2012

Surveillance records of the acute RNA pathogen of Pacific salmonid fish infectious hematopoietic necrosis virus are combined for the first time to enable landscape-level ecological analyses and modeling. The study area is the freshwater ecosystems of the large Columbia River watershed in the U.S. states of Washington, Oregon, and Idaho, as well as coastal rivers in Washington and Oregon. The study period is 2000–2012, and records were contributed by all five resource management agencies that operate conservation hatcheries in the study area. Additional records from wild fish were collected from the National Wild Fish Health Survey, operated by the U.S. Fish and Wildlife Survey. After curation and normalization, the data set consists of 6766 records, representing 1146 sample sites and 15 different fish hosts. The virus was found in an average of 12.4% of records, and of these 66.2% also have viral genetic analysis available. This data set is used to conduct univariate ecological and epidemiological analyses and develop a novel hierarchical landscape transmission model for an aquatic pathogen.

Ecology

Molecular characterization of a novel orthomyxovirus from rainbow and steelhead trout ( Oncorhynchus mykiss )

A novel virus, rainbow trout orthomyxovirus (RbtOV), was isolated in 1997 and again in 2000 from commercially-reared rainbow trout ( Oncorhynchus mykiss ) in Idaho, USA. The virus grew optimally in the CHSE-214 cell line at 15°C producing a diffuse cytopathic effect; however, juvenile rainbow trout exposed to cell culture-grown virus showed no mortality or gross pathology. Electron microscopy of preparations from infected cell cultures revealed the presence of typical orthomyxovirus particles. The complete genome of RbtOV is comprised of eight linear segments of single-stranded, negative-sense RNA having highly conserved 5′ and 3′-terminal nucleotide sequences. Another virus isolated in 2014 from steelhead trout (also O. mykiss ) in Wisconsin, USA, and designated SttOV was found to have eight genome segments with high amino acid sequence identities (89–99%) to the corresponding genes of RbtOV, suggesting these new viruses are isolates of the same virus species and may be more widespread than currently realized. The new isolates had the same genome segment order and the closest pairwise amino acid sequence identities of 16–42% with Infectious salmon anemia virus (ISAV), the type species and currently only member of the genus Isavirus in the family Orthomyxoviridae . However, pairwise comparisons of the predicted amino acid sequences of the 10 RbtOV and SttOV proteins with orthologs from representatives of the established orthomyxoviral genera and a phylogenetic analysis using the PB1 protein showed that while RbtOV and SttOV clustered most closely with ISAV, they diverged sufficiently to merit consideration as representatives of a novel genus. A set of PCR primers was designed using conserved regions of the PB1 gene to produce amplicons that may be sequenced for identification of similar fish orthomyxoviruses in the future.

Virus Research

Complete sequences of 4 viral hemorrhagic septicemia virus IVb isolates and their virulence in northern pike fry

Four viral hemorrhagic septicemia virus (VHSV) genotype IVb isolates were sequenced, their genetic variation explored, and comparative virulence assayed with experimental infections of northern pike Esox lucius fry. In addition to the type strain MI03, the complete 11183 bp genome of the first round goby Neogobius melanostomus isolate from the St. Lawrence River, and the 2013 and 2014 isolates from gizzard shad Dorosoma cepedianum die-offs in Irondequoit Bay, Lake Ontario and Dunkirk Harbor, Lake Erie were all deep sequenced on an Illumina platform. Mutations documented in the 11 yr since the MI03 index case from Lake St. Clair muskellunge Esox masquinongy showed 87 polymorphisms among the 4 isolates. Twenty-six mutations were non-synonymous and located at 18 different positions within the matrix protein, glycoprotein, non-virion protein, and RNA polymerase genes. The same 4 isolates were used to infect northern pike fry by a single 1 h bath exposure. Cumulative percent mortality varied from 42.5 to 62.5%. VHSV was detected in 57% (41/72) of the survivors at the end of the 21-d trial, suggesting that the virus was not rapidly cleared. Lesions were observed in many of the moribund and dead northern pike, such as hemorrhaging in the skin and fins, as well as hydrocephalus. Mean viral load measured from the trunk and visceral tissues of MI03-infected pike was significantly higher than the quantities detected in fish infected with the most recent isolates of genotype IVb, but there were no differences in cumulative mortality observed.

Diseases of Aquatic Organisms

Increasing virulence, but not infectivity, associated with serially emergent virus strains of a fish rhabdovirus

Surveillance and genetic typing of field isolates of a fish rhabdovirus, infectious hematopoietic necrosis virus (IHNV), has identified four dominant viral genotypes that were involved in serial viral emergence and displacement events in steelhead trout ( Oncorhynchus mykiss ) in western North America. To investigate drivers of these landscape-scale events, IHNV isolates designated 007, 111, 110, and 139, representing the four relevant genotypes, were compared for virulence and infectivity in controlled laboratory challenge studies in five relevant steelhead trout populations. Viral virulence was assessed as mortality using lethal dose estimates (LD50), survival kinetics, and proportional hazards analysis. A pattern of increasing virulence for isolates 007, 111, and 110 was consistent in all five host populations tested, and correlated with serial emergence and displacements in the virus-endemic lower Columbia River source region during 1980–2013. The fourth isolate, 139, did not have higher virulence than the previous isolate 110. However, the mG139M genotype displayed a conditional displacement phenotype in that it displaced type mG110M in coastal Washington, but not in the lower Columbia River region, indicating that factors other than evolution of higher viral virulence were involved in some displacement events. Viral infectivity, measured as infectious dose (ID50), did not correlate consistently with virulence or with viral emergence, and showed a narrow range of variation relative to the variation observed in virulence. Comparison among the five steelhead trout populations confirmed variation in resistance to IHNV, but correlations with previous history of virus exposure or with sites of viral emergence varied between IHNV source and sink regions. Overall, this study indicated increasing viral virulence over time as a potential driver for emergence and displacement events in the endemic Lower Columbia River source region where these IHNV genotypes originated, but not in adjacent sink regions.

Virus Evolution

Phylogenetic relationships of Iranian infectious hematopoietic necrosis virus of rainbow trout (Oncorhynchus mykiss) based on the glycoprotein gene

Infectious hematopoietic necrosis virus (IHNV), a member of family Rhabdoviridae and genus Novirhabdoviridae, causes a highly lethal disease of salmon and trout. In Iran IHNV was first detected in 2001 on farms rearing rainbow trout (Oncorhynchus mykiss). To evaluate the genetic relationships of IHNV from northern and western Iran, the sequences of a 651-nt region of the glycoprotein gene were determined for two Iranian isolates. These sequences were analyzed to evaluate their genetic relatedness to worldwide isolates representing the five known genogroups of IHNV. Iranian isolates were most closely related to European isolates within the genogroup E rather than those of North American genogroups U, M and L, or the Asian genogroup J. It appears that Iranian IHNV was most likely introduced to Iran from a source in Europe by the movement of contaminated fish eggs.

Archives of Virology

Emergence of MD type infectious hematopoietic necrosis virus in Washington State coastal steelhead trout

Infectious hematopoietic necrosis virus (IHNV) occurs in North America as 3 major phylogenetic groups designated U, M, and L. In coastal Washington State, IHNV has historically consisted of U genogroup viruses found predominantly in sockeye salmon Oncorhynchus nerka . M genogroup IHNV, which has host-specific virulence for rainbow and steelhead trout O. mykiss , was detected only once in coastal Washington prior to 2007, in an epidemic among juvenile steelhead trout in 1997. Beginning in 2007 and continuing through 2011, there were 8 IHNV epidemics in juvenile steelhead trout, involving 7 different fish culture facilities in 4 separate watersheds. During the same time period, IHNV was also detected in asymptomatic adult steelhead trout from 6 coastal watersheds. Genetic typing of 283 recent virus isolates from coastal Washington revealed that the great majority were in the M genogroup of IHNV and that there were 2 distinct waves of viral emergence between the years 2007 and 2011. IHNV type mG110M was dominant in coastal steelhead trout during 2007 to 2009, and type mG139M was dominant between 2010 and 2011. Phylogenetic analysis of viral isolates indicated that all coastal M genogroup viruses detected in 1997 and 2007 to 2011 were part of the MD subgroup and that several novel genetic variants related to the dominant types arose in the coastal sites. Comparison of spatial and temporal incidence of coastal MD viruses with that of the rest of the Pacific Northwest indicated that the likely source of the emergent viruses was Columbia River Basin steelhead trout.

Washington