Language selection

Government of Canada / Gouvernement du Canada

Search

Herpes-Type Virus Disease of Oysters

On this page

Category

Category 1 (Not Reported in Canada)

Common, generally accepted names of the organism or disease agent

Herpes-type virus disease, Ostreid Herpesvirus type 1 (OsHV-1) which may be, in some cases, the undiagnosed cause of the disease called summer mortalities of Crassostrea gigas (Guo and Ford 2016). In Australia, the acronym POMS (Pacific Oyster Mortality Syndrome) was created to refer to mass mortalities due to OsHV-1 (Paul-Pont et al. 2013a).

Scientific name or taxonomic affiliation

Herpes-type virus or herpes-like viruses. Ostreid Herpesvirus type 1 (OsHV-1) from Crassostrea gigas in France has been described and represents a major class of herpesviruses that is different from those in vertebrates (Davison et al. 2005, Renault 2008a). Like other herpesviruses, OsHV-1 is a double-stranded DNA virus. It was placed in the order Herpesvirales, family Malacoherpesviridae and genus Ostreavirus (Davison 2010, Renault 2011, 2016) and species Ostreid Herpesvirus 1 (see the International Committee on Taxonomy of Viruses web site). The apparent lack of host specificity in bivalves and loss of several gene functions in OsHV-1 prompted speculation that this virus may have resulted from interspecies transmission in the context of introduction and intensive culture of non-native bivalve species (Arzul et al. 2001a, b). It is not known if all herpes-like viruses reported from various species of oysters and other bivalves are the same or different species of herpesvirus. However, variations among DNA sequences of OsHV-1 have been reported (Arzul et al. 2001c, 2017; Friedman et al. 2005; Moss et al. 2007; Barbosa Solomieu et al. 2015; Martenot et al. 2015a; Bai et al. 2015; Morrissey et al. 2015; Rosani and Venier 2017). Segarra et al. (2010) described the microvariant OsHV-1 μVar from several locations in France. This variant apparently spread rapidly around the world (Martenot 2013) but it primarily infects C. gigas (Alfjorden et al. 2017). Between 2008 and 2010, Martenot et al. (2011) characterized the genotype (variants or OsHV-1 reference) of 300 positive samples from C. gigas collected along the French, Jersey, and Irish coasts and reported that the majority of samples (257) were characterized as OsHV-1 μVar. The genotype OsHV-1 reference was never detected and a novel genotype named OsHV-1 μVar Δ9 was found in 5 samples from Normandy, France (Martenot et al. 2011). Subsequently, Martenot et al. (2012, 2013, 2015a), Renault et al. (2012), Lynch et al. (2012) and Morrissey et al. (2015) reported additional microvariants (virus type) of OsHV-1 from France, Ireland and other locations around the world including China (Bai et al. 2015), and the Adriatic Sea, Italy (Abbadi et al. 2018). The pathogenicity of a Japanese variant named OsHV-1 JPType 1 was studied in C. gigas larvae and spat in Japan (Nagai and Nakamori 2018). Arzul et al. (2017) presented detailed information on the genetic diversity reported in OsHV-1. The European Food Safety Authority (EFSA) Panel on Animal Health and Welfare (AHAW) (EFSA (AHAW) 2015) determined that almost all OsHV-1 strains isolated after 2008 conformed to the definition of microvariants and therefore, it appeared unnecessary to maintain a separate definition of microvariants for disease control purposes. In addition to other species of bivalves (see below), herpes-like viruses have been reported from abalone.

Because some of the herpes-like viruses reported in various species of oysters (and other bivalves) have not been specifically identified, the reports presented below were grouped according to main host/geographic region and listed alphabetically. Each reported geographic location and host species was consistently assigned the same letter code with the classical OsHV-1 listed in position 'a'. The remainder of the topics (i.e., impact on host, diagnostic techniques, and methods of control) focus on OsHV-1.

Geographic distribution

Mineur et al. (2015) compiled molecular data on OsHV-1 to infer an Asian geographical origin for ostreid herpesviruses which are now wide spread and can be pathogenic under farming conditions. Details of geographic reports are as follows:

  1. Oyster mortalities associated with herpesvirus were first reported from oyster larvae in hatcheries in New Zealand (Hine et al. 1992) and hatchery-reared oyster larvae and juveniles (including spat) in France (Nicolas et al. 1992). OsHV-1, OsHV-1 μVar, and/or variant genotypes closely related to the OsHV-1 μVar were also detected in juvenile C. gigas (often associated with high mortality events) farmed:
    • in Italy (Dundon et al. 2011, Domeneghetti et al. 2014),
    • on the Mediterranean coast of France (Pernet et al. 2012),
    • on the Mediterranean and Atlantic coasts of Spain (Roque et al. 2012, Aranguren et al. 2012, López-Sanmartín et al. 2016a),
    • in the Netherlands (Gittenberger et al. 2016),
    • in Jersey (Martenot et al. 2011),
    • in Ireland (Peeler et al. 2012, Lynch et al. 2012, Clegg et al. 2014, Morrissey et al. 2015) and some areas of the United Kingdom (Barbosa Solomieu et al. 2015) but not Scotland (Murray et al. 2012),
    • in Sweden and Norway (ICES 2018, Mortensen et al. 2016),
    • in New South Wales and Tasmania, Australia (Paul-Pont et al. 2013a, b, 2014; Jenkins et al. 2013; de Kantzow et al. 2017),
    • in Korea (Hwang et al. 2013) and in samples obtained from China, Japan and New Zealand (Renault et al. 2012, Shimahara et al. 2012, Keeling et al. 2014, Bai et al. 2015).

    Barbieri et al. (2019) reported this virus associated with lesions in the mantle tissues of adult C. gigas in the Bahia Blanca Estuary, Argentina. In Japan, Shimahara et al. (2012) found variable types of OsHV-1 but their nucleotide sequences were not identical to those of OsHV-1 μVar and Nagai and Nakamori (2018) investigated the pathogenicity of one of them (OsHV-1 JPType 1) in C. gigas. A closely related virus was detected in juvenile C. gigas in California, USA (Friedman et al. 2005; Burge et al. 2006, 2011; Burge 2010) and in the eroded gills of adult C. gigas along the northwestern Pacific coast of Baja California, Mexico (Vásquez-Yeomans et al. 2004, 2010). Grijalva-Chon et al. (2013) detected a new OsHV-1 DNA strain using molecular assays in healthy, juvenile and adult, C. gigas from the Gulf of California, Mexico without visual confirmation of infection (for example: histology, transmission electron microscopy, and/or  in-situ hybridization were not conducted). In Portugal, OsHV-1 μVar was detected in adult Crassostrea angulate experiencing a 47 to 59% mortality outbreak (Batista et al. 2015). Alfjorden et al. (2017) indicated that OsHV-1 was also reported in Brazil, Morocco and Tunisia. Using only PCR assays on adult oysters with no associated mortalities, Mello et al. (2018) confirmed the presence of OsHV-1 on the coast of Santa Catarina, Brazil. Arzul et al. (2017) speculated that based on phylogenetic relationships, the OsHV-1 µVar variant reported in Europe since 2008 may be derived from virus specimens originating from the Pacific area.

  2. Coastal waters of Maine and New York, USA (Farley et al. 1972, Farley 1978).
  3. Various locations in Europe including: France (Comps and Cochennec 1993, Renault et al. 2000a, Renault and Arzul 2001); the United Kingdom (Davison et al. 2005); and in juvenile oysters from various stocks grown experimentally in Galicia, Spain (da Silva et al. 2008).
  4. Tasmania and Western Australia (Hine and Thorne 1997).
  5. New Zealand (Hine et al. 1992, 1998).
  6. Asia including Japan, South Korea and China (Moss et al. 2007, Shimahara et al. 2012, Bai et al. 2015).
  7. Alaska, USA (Meyers et al. 2009).

Host species

In molluscs, herpes-like viruses, including Ostreid Herpesvirus type 1 (OsHV-1), have a broad host range. In addition to oyster hosts mentioned below, herpes-like viruses have been reported in clams, scallops and abalone (Guo and Ford 2016), and mussels which were reported to be less susceptible than Crassostrea gigas (Novoa et al. 2016). Experimental trials showed that a similar genotype of OsHV-1 could induce an infection at larval stages in different bivalve species and that interspecies transmission could occur (Arzul et al. 2001a, b, c, 2017). The following information includes only reports from oysters.

  1. Most of the early virus identity studies of OsHV-1 were conducted on isolates from C. gigas in France (Renault 2006, Segarra et al. 2010). Details on reports of host species for this virus in oysters are as follows:
    • isolates from C. gigas larvae in France were determined to be infective to larvae of other species of oyster (Crassostrea angulata, Crassostrea rivularis and Ostrea edulis) under experimental conditions (Arzul et al. 2001a, b) and in bivalve hatcheries (Renault and Arzul 2001; Renault et al. 2000a, 2001)
    • in asymptomatic adult C. gigas in France (Arzul et al. 2002);
    • in healthy spat and juvenile C. gigas, Crassostrea ariakensis and Crassostrea sikamea in Japan (Shimahara et al. 2012)
    • in apparently healthy young adult C. gigas, C. angulata and their F1 hybrids in Portugal (Batista et al. 2014)

    Subsequently, OsHV-1 μVar was detected in dying adult C. angulata in Portugal (Batista et al. 2015), in apparently healthy Ostrea stentina in SW Spain (López-Sanmartín et al. 2016a) and transmitted experimentally to O. edulis (López-Sanmartín et al. 2016b). In New South Wales, Australia, low levels of OsHV-1 with no associated mortality were detected by quantitative PCR but not by in situ hybridisation in Saccostrea glomerata growing adjacent to C. gigas that were experiencing high mortalities (greater than 95%) and had heavy loads of OsHV-1 (Jenkins et al. 2013). Burge et al. (2011) detected related oyster herpesvirus (OsHV) DNA in asymptomatic C. gigas, C. sikamea, Crassostrea virginica, O. edulis. Tan et al. (2015) determined that under the conditions of the experimental challenge, the black-lip pearl oyster Pinctada margaritifera was not sensitive to OsHV-1 μVar and was not an effective host/carrier. Using only PCR assays on adult oysters with no associated mortalities, Mello et al. (2018) detected OsHV-1 in Crassostrea brasiliana (=C. gasar) from the southern coast of Brazil.

  2. Crassostrea virginica (Farley et al. 1972, Farley 1978).
  3. Ostrea edulis (Comps and Cochennec 1993, da Silva et al. 2008).
  4. Ostrea angasi (Hine and Thorne 1997).
  5. Larvae of C. gigas (Hine et al. 1992) and Ostrea (=Tiostrea) chilensis (Hine et al. 1998) from hatcheries in New Zealand near Auckland and Wellington, respectively. A subsequent survey of 885 molluscs (9 species of bivalves and 1 species of gastropod) from various locations around New Zealand did not detect OsHV-1 (Webb et al. 2007).
  6. Crassostrea ariakensis, C. gigas, C. sikamea, and Crassostrea hongkongensis (Moss et al. 2007, Shimahara et al. 2012). 
  7. Morphological structures (observed by histology and transmission electron microscopy) similar to those of the herpesvirus-like agent were detected in C. gigas in Alaska (Meyers et al. 2009).

Impact on the host

Herpes-like viruses in oysters were first reported in Crassostrea virginica that died in cages under conditions of elevated water temperatures (28 to 30ºC) in Maine, USA (Farley et al. 1972, Guo and Ford 2016). About 20 years later, in 1991 and 1993, the first herpes-like virus outbreaks in Europe were associated with high mortalities (80 - 90%) among Crassostrea gigas larvae in oyster hatcheries and juveniles (spat, 3 to 7 months old), respectively, in France (Nicolas et al. 1992; Renault et al. 1994a, b; Guo and Ford 2016). The disease quickly spread among C. gigas larvae in commercial hatcheries in France, indicating a short productive cycle for the virus, with cumulative mortalities approaching 100% within a few days. Also in 1991, herpes virsus were associated with high mortalities in hatcher-reared C. gigas larvae in New Zealand (Hine et al. 1992, Guo and Ford 2016). Between 1998 and 2002, herpes-like viruses were reported from an increasing number of larval bivalve species from around the world, especially in Europe, and are now thought to be ubiquitous with associated substantial mortalities in hatcheries (Renault et al. 2000, 2001; Coen and Bishop 2015). Arzul et al. (2001a, b, c) showed that the Ostreid Herpesvirus type 1 (OsHV-1) from C. gigas can infect several bivalve species and Davison (2005) analysed the capsid morphology and genome sequence of OsHV-1 in order to assess its relationship to vertebrate herpesviruses. Guo and Ford (2016) noted that in France, the OsHV-1 outbreaks in C. gigas followed a period of rapid expansion of the oyster aquaculture industry. They speculated that large-scale aquaculture at high densities, or ocean warming, or both could have contributed to the large-scale epizootics of OsHV-1 in oysters.

Since 2008, massive mortality outbreaks were reported in several C. gigas oyster farms in France, Ireland, the United Kingdom, the Ebro Delta area of Spain, and Australia. The outbreaks were associated with a particular variant of OsHV-1, called OsHV-1 μVar and were attributed to adverse environmental conditions (especially a rise in water temperatures (+0.5°C/day, > 4 days) and/or other factors such as toxic phytoplankton blooms or the presence of a pathogenic Vibrio sp., etc.) (Renault 2011, Saulnier et al. 2011, Jenkins et al. 2013, Domeneghetti et al. 2014, Barbosa Solomieu et al. 2015, Carrasco et al. 2017). In 2010, a panel of the European Food Safety Authority suggested that OsHV-1 infection is a necessary cause but may not be a sufficient cause of the severe mortality events of 2008 and 2009 in cultured juvenile C. gigas in Europe, and the strain OsHV-1 μVar seemed to be dominant (EFSA (AHAW) 2010).

In Italy in 2010, OsHV-1 and the microvariant (OsHV-1 μVar) were detected in juvenile C. gigas during grow-out despite the absence of clinical and pathological signs normally associated with the presence of this variant (Dundon et al. 2011). However, in France, OsHV-1 viral DNA detection was negligible except during mortality events and its prevalence and intensity in C. gigas tissues increased rapidly just before and during mortality outbreaks (Saulnier et al. 2011, Dégremont 2011). Garcia et al. (2011) also suspected that OsHV-1 was associated with oyster mortalities but indicated that subsequent work, particularly epidemiological surveys, would be useful to confirm the causal link between the detection of OsHV-1 and the mortality outbreaks in juvenile C. gigas.

Burge et al. (2020)noted that isolates of OsHV-1 µVar from Australia and France produced similar disease in C. gigas. Specifically, in bath exposure experiments, juvenile C. gigas (about 9 mm shell length) were relaxed and exposed for 2 hours to isolates of OsHV-1 µVar from Australia or France, the oyster spat had similar low survival (2.5% and 10%, respectively) and high viral copy numbers. Bath exposure experiments were also used by Agnew et al. (2020) to assess the resistance of juvenile C. gigas (6 to 8 mm in shell length) from the USA west coast Molluscan Broodstock Program (de Melo et al. 2016) to 3 variants of OsHV-1, specifically, a California, USA reference OsHV-1 and isolates of OsHV-1 µVar from Australia and France. Results indicated that the survival probability of oysters exposed to the French or Australian OsHV-1 µVar was significantly lower (43% and 71%, respectively) than to the California reference variant and controls (96%). These results highlight the need to consider differences in virulence among variants when testing oyster stocks for resistance to OsVH-1 (Agnew et al. 2020).

The pathogenicity of OsHV-1 may be related to poor husbandry such as crowding and the disease is most prevalent during the summer periods. This pathogen (in conjunction with other pathogens, environmental factors (such as elevated temperatures, physiological stress associated with gonadal maturation, aquaculture practices, water quality, predators, phytoplankton blooms, food quality, etc.), and genetic factors has been associated with the syndrome known as 'summer mortality' which severely affects the aquaculture production of C. gigas in many countries including Japan; Pacific Northwest, USA; Australia; Ireland; and France (Sauvage et al. 2010, Carnegie 2011, Lynch et al. 2012, Fleury and Huvet 2012, Pernet et al. 2014). The term "summer mortality" was typically associated with prolonged losses that affect older, reproductively mature animals (Burge 2010). However, various studies have investigated the role of OsHV-1 and variants as causative agents in C. gigas summer mortalities and have found this virus to be particularly associated with larval and juvenile mortalities (Comps and Cochennec 1993; Renault et al. 1994a, b, 2000a; LeDeuff and Renault 1999; Friedman et al. 2005; Burge et al. 2006, 2007; Miossec et al. 2009; Lynch et al. 2012; Peeler et al. 2012; Degremont and Benabdelmouna 2014; Pernet et al. 2014). For example, in France, Oden et al. (2011) detected high concentrations of OsHV-1 (5×107 DNA copies per 50 mg of dying juvenile C. gigas tissue as measured using a molecular assay) that were associated with summer mortality occurrence. Dégremont (2011) also reported an association between summer mortality in juvenile C. gigas and OsHV-1 in Marennes-Oléron Bay, France.

The role of other pathogenic agents such as Vibrio spp. in disease associated with OsHV-1 has not yet been fully resolved (EFSA (AHAW) 2010, Barbosa Solomieu et al. 2015). For example, Saulnier et al. (2011) and Dégremont (2011) indicated that bacteria belonging to the Vibrio splendidus group and Vibrio aestuarianus were frequently detected in the living spat but the intensity of bacteria in the tissues did not significantly increase during periods of increased mortality. Petton et al. (2015a) found no correlation between Vibrio spp. concentration and OsHV-1 load (DNA concentration determined by molecular assays) in co-infected animals and the quantity of viral DNA was a predictor of mortality. However, in the absence of bacteria, a high load of herpesvirus was not sufficient to induce the full expression of the disease (Petton et al. 2015a). Selection of C. gigas with resistance to OsHV-1 seemed to provide resistance to V. aestuarianus at the juvenile stage of oyster development but did not benefit adult oysters (Azema et al. 2015c). It is important to note that mortality related to V. aestuarianus tends to increase with oyster size and age (Azema et al. 2015a, Moreau et al. 2015b). Also, Azema et al. (2017) determined that there was no genetic correlations in C. gigas between resistance to OsHV-1 infection and resistance to V. aestuarianus infection. Such investigations emphasize the complexity of the molluscan immune response as further discussed by Agius et al. (2020).

Several epidemiological investigations conducted since 2011 have revealed various factors associated with disease caused by OsHV-1 (Arzul et al. 2017). In experimental field studies, Dégremont (2011, 2013), Jenkins et al. (2013) and Whittington et al. (2015b) determined that mortalities can be attributed to OsHV-1 alone because of the pattern of mortalities and the presence of a high viral load of OsHV-1 in moribund juvenile C. gigas sampled during peak mortality. However, de Lorgeril et al. (2018) determined that the disease is caused by multiple infections with an initial and necessary step of infection of oyster haemocytes by OsHV-1 µVar which leads to the host entering an immune-compromised state, evolving towards subsequent bacteraemia by opportunistic bacteria. In Europe, Dégremont (2013) reported that all mortalities occurred when seawater temperature was above 16°C, which was termed the 'risk' period. For all deployments made during the risk period, mortality was observed within 2 weeks post-deployment and most episodes lasted over a week. For deployments made outside of the risk period, mortality occurred as soon as the next risk period began (Dégremont 2013). Renault et al. (2014a) detected a similar correlation between juvenile C. gigas mortality associated with OsHV-1 and increases in water temperature. In Australia, Jenkins et al. (2013) also reported that the sentinel triploid C. gigas (60 mm shell height) quickly became infected and experienced nearly 100% mortality within 2 weeks of exposure. Paul-Pont et al. (2014) found that although seawater temperatures were consistently above 24°C (±3°C) during the month preceding mass mortalities in farmed juvenile triploid C. gigas, high temperatures did not necessarily lead to mortality events when the virus was present. The incubation period for mass mortality was less than 4 days, however subclinical OsHV-1 infection was detected 3 months prior to the first signs of mortality in the index case site (first location affected), which suggests that low viral loads of OsHV-1 are insufficient to induce the disease (Paul-Pont et al. 2014). Rapidity of onset and virulence of OsHV-1 in naïve C. gigas spat was also reported in New Zealand waters (Keeling et al. 2014).

In agreement with field observations in Europe, Petton et al. (2013) determined that the optimal temperature range for disease transmission from field-exposed C. gigas to naïve juvenile C. gigas in the laboratory was between 16.2 and 21.9°C and that no transmission occurred at temperatures less than 13°C. De Kantzow et al. (2016, 2020) also used laboratory experiments to identify a threshold water temperature of between 14 and 18ºC and confirmed a direct effect of water temperature on infection and disease caused by OsHV-1 μVar. Green et al. (2014a) speculated that at 22ºC juvenile C. gigas produced a vigorous antiviral response that resulted in an immune-mediated disorder causing mortality. Delisle et al. (2018), assessing how temperature modulates C. gigas susceptibility to OsHV-1 and pathogen virulence, determined that high temperature (29°C) decreased the susceptibility of oysters to OsHV-1 without altering virus infectivity and virulence and overall survival of oysters infected at 29°C remained higher than oysters infected at 21°C and 26°C.

During investigations into the interactive effects of temperature and disease exposure on physiological parameters of juvenile C. gigas, Tamayo et al. (2014) suggested that although energetic reserves were being diminished in infected oysters, their metabolic activities remained similar to that of healthy animals. Also in the laboratory, Schikorski et al. (2011b) demonstrated that healthy one-year old C. gigas (about 40 mm in length), after 2 days of cohabitation with oysters experimentally infected by injection, develop the disease with mortality rates increasing gradually for the first 8 days and reached a maximum of about 50% by day 8. At 6 hours after cohabitation exposure, haemocytes contained more viral DNA than the gills, mantle, adductor muscle and digestive gland (Schikorski et al. 2011b). Similar results in laboratory experiments were also obtained by Evans et al. (2015, 2017a) and Morga et al. (2017).

Various other factors that seem to affect the possibilities of infection and outcome of the disease have been reported. For example:

  1. Lassudrie et al. (2015) indicated that exposure to the harmful dinoflagellate Alexandrium catenella modified the host–pathogen interaction by reducing prevalence of OsHV-1 μVar infection in C. gigas spat. In addition, oysters challenged with OsHV-1 μVar and possibly other pathogens from the environment accumulated smaller amounts of Paralytic Shellfish Toxins than unchallenged oysters. The authors suggested 3 possible mechanisms for these results:
    • possible direct interactions between A. catenella and herpesvirus (or associated pathogens) could reduce viral transmission and algal availability for oyster consumption
    • oyster feeding behavior or digestive functions may have been altered, thus decreasing both uptake of viral particles and consumption or digestion of toxic algae and consequent toxin accumulation
    • immuno-activation by A. catenella could enhance defense efficiency against OsHV-1 μVar infection (Lassudrie et al. 2015).

  2. Moreau et al. (2015a) determined that pesticides at realistic concentration exerted adverse effects on C. gigas and caused an increased susceptibility to the OsHV-1 infection in experimental conditions.

  3. Martenot et al. (2015b) indicated that infectious OsHV-1 μVar stability in seawater was modulated by temperature and elevated water temperatures (25°C for over 33 hours) were not favorable for virus survival. Other water quality parameters, such as lower-alkalinity seawater, may be important for OsHV-1 transmission because it may influence the duration of viral viability outside of the oyster (Burge et al. 2020).
  4. Schikorski et al. (2011a) demonstrated that filtered (0.22 μm) tissue homogenates prepared from naturally OsHV-1 μVar infected spat collected on the French coast during mortality outbreaks in 2008 induced mortalities by intramuscular injection into healthy juvenile C. gigas (about 40 mm in length and 5 grams wet weight). However, the same tissue homogenates exposed to an ultraviolet (UV) treatment did not induce any mortality suggesting that juvenile oyster mortalities caused by OsHV-1 require the presence of a UV sensitive agent (Schikorski et al. 2011a).

  5. Age and size seem to affect susceptibility of oysters to OsHV-1 with oysters less than 1 year of age being more susceptible and larger oysters are more resistant to viral infection (Renault et al. 1995, Miossec et al. 2009, Schikorski et al. 2011a, Garcia et al. 2011, Peeler et al. 2012, Normand et al. 2014, Whittington et al. 2015b, Hick et al. 2018).

  6. Prior exposure to the virus has a protective effect (Arzul et al. 2017). For example, spat originating from an endemic region of OsHV-1 μVar displayed less mortality than spat from a free zone (Clegg et al. 2014) and unexposed spat showed a rapid viral replication and a quick increase of mortality (Keeling et al. 2014) when the spat were deployed into an endemic region.

  7. Salinity of 25 ppt increased C. gigas mortality associated with OsHV-1 especially when oysters were not previously acclimated and low salinity (10 ppt) decreases OsHV-1 infectivity (Fuhrmann et al. 2016). Further studies indicated that metabolism in C. gigas is influenced by salinity and oysters with a higher antioxidant activity and a better physiological condition seemed less susceptible to OsHV-1 (Fuhrmann et al. 2018).

Horizontal transmission (between individuals in a population) seems to be the usual mechanism of spread of OsHV-1. For example, Degremont and Benabdelmouna (2014) demonstrated that OsHV-1 was horizontally transmitted from the wild-caught C. gigas spat to the hatchery-produced C. gigas. Paul-Pont et al. (2013b) determined that the distribution of OsHV-1 associated mortalities was spatially clustered, highly variable and clearly dependent on the age of oysters and their position in the water column with hydro-dynamics, physical disturbances, host density/distribution, and variations of environmental parameters thought to influence the mechanism of disease transmission. They hypothesized that OsHV-1 may be carried through water by particles, possibly by planktonic organisms, which may also explain the patchy distribution of mortalities (Paul-Pont et al. 2013b). In large-scale aquaculture facilitates, OsHV-1 outbreaks deserves attention because of the important implications for future aquaculture developments and the management of marine diseases (Pernet et al. 2016, Guo and Ford 2016).

Vertical transmission of OsHV-1 (from adults to larvae) has been implicated for asymptomatic oysters (in C. gigas by Le Deuff et al., (1996) and Arzul et al. (2002) and in O. edulis by da Silva et al. (2008)). López-Sanmartín et al. (2016c) determined that C. angulate that have survived an OsHV-1 mortality outbreak can carry the virus and vertically transmit it to their offspring. In adult oysters, the connective tissue of the gonad was among the regions that contained infected cells (Arzul et al. 2002). Barbosa-Solomieu et al. (2005) detected OsHV-1 in 3 successive generations of C. gigas including 2 day-old larvae. Crosses involving an OsHV-1 infected male and a non-infected female resulted in hatching and larval survival rates statistically lower than those observed in the other types of crosses suggesting that OsHV-1 infected females may transmit to their offspring some kind of protection or resistance against viral infection (Barbosa-Solomieu et al. 2005). Evans et al. (2017a) reported that the prevalence and intensity of OsHV-1 in older C. gigas, which had been exposed to OsHV-1 in prior seasons, were consistently low (< 10% prevalence and <104 DNA copies per mg tissue or μL haemolymph, respectively) and suggested that such oysters may not be a major reservoir host of the virus for subsequent outbreaks. However, Evans et al. (2017a) cautioned that further investigations are required to ascertain whether OsHV-1 replication occurs in surviving oysters, and whether transmission from them to naive oysters and induction of clinical disease is possible.

Crassostrea gigas is capable of defending itself from disease caused by OsHV-1. Adult C. gigas that appear normal (healthy) can be infected with OsHV-1 (Arzul et al. 2002, Batista et al. 2014, Evans et al. 2017a) and experimental results indicated that some juvenile C. gigas are capable of developing a strong and complex antiviral response (He 2015, Guo and Ford 2016, Green and Speck 2018, Agius et al. 2020). In a review of antiviral activity in marine molluscs, Green et al. (2015a) indicted that antiviral defences can be enhanced by genetic selection, as shown by the presence of oyster strains specifically resistant to OsHV-1. Green and Montagnani (2013) demonstrated that juvenile C. gigas (mean weight of 3.8 grams) can recognise double-strand RNA to initiate an innate immune response that inhibits viral infection with OsHV-1 μVar. Green et al. (2014b) provided evidence that cavortin, a multifunctional protein involved in immunity, was associated with this antiviral activity in C. gigas. Allam and Raftos (2015) and Agius et al. (2020) reviewed the subject of antiviral activity (immunity) in bivalves. The immune response to OsHV-1 and resistance to mortality caused by OsHV-1 increased with both age and size of C. gigas suggesting a maturation of the immune system against the virus (Green et al. 2016a, Arzul et al. 2017). In field conditions, the relationship between mortality and size was stronger than the relationship between mortality and age (Dégremont 2013). In Australia, mortalities associated with OsHV-1 were recorded in all age classes of C. gigas but were greater in spat and juveniles than in adults (Paul-Pont et al. 2014). Apoptosis, the autophagy pathway and other mechanisms are likely involved in disease resistance in juvenile and adult C. gigas (Segarra et al. 2014a, Moreau et al. 2015b, Green et al. 2015b, Aguis et al. 2020). Although increased susceptibility of juvenile oysters was initially hypothesized to be due to an immature immune system incapable of mounting an effective response to OsHV-1 (e.g., Jenkins et al. 2013), Aguis et al. (2020) suggested that juveniles actually mount an 'over the top' and perhaps unregulated immune response, which may create a toxic cellular environment ultimately resulting in their death.

Pepin et al. (2008) confirmed the high genetic basis underlying the variance of resistance of C. gigas to OsHV-1. Renault et al. (2011) identified virus-induced genes in C. gigas haemocytes that were challenged with OsHV-1. Jouaux et al. (2013) developed a microarray assay for a major part of the oyster genome and determined that a number of genes regulate the response to OsHV-1 infection. Gómez-Chiarri et al. (2015) indicated that analysis using –omic tools (genomic, metagenomic, epigenomic, transcriptomic,and proteomic) are currently limited but their expansion for studies focused on bivalve disease processes (including those involving OsHV-1) should be facilitated as more transcriptome datasets and complete genome sequences become available for marine bivalve species. For example, Corporeau et al. (2014) suggested that the results of proteomic analysis should be useful for identifying potential biomarkers of disease resistance and developing antiviral measures to OsHV-1 infection. Rosani et al. (2015) performed a dual RNA sequencing analysis on a sample of C. gigas spat with a high viral load of OsHV-1 to identify several highly induced and defence-related oyster transcripts which support the role played by the innate immune system against the virus.

Meyers (1981) reported an apparent herpesvirus infection, with no associated disease, in 1 of 243 adult C. virginica from the south shore of Long Island, New York. In Western Austraila, Hine and Thorne (1997) detected intranuclear inclusions associated with herpes-like viruses in haemocytes of 23% of the adult O. angasi population that was experiencing low level mortalities associated with Bonamia sp. but with no apparent mortalities attributable to the viral infection. In New South Wales, Australia, Jenkins et al. (2013) suggested that Saccostrea glomerata is not susceptible to infection with OsHV-1 because mortalities were not evident and molecular assays (quantitative PCR and in situ hybridisation) were negligible for the virus while neighbouring C. gigas were experiencing high mortalities (greater than 95%) and had high loads of OsHV-1. Nevertheless, Evans et al. (2017b) detected low levels of OsHV-1 in apparently healthy S. glomerata from several sites in the Georges River estuary, New South Wales, Australia. In O. chilensis larvae and spat from New Zealand, the interstitial cells, mantle and digestive tract epithelial cells were infected with a herpesvirus and infection appeared to be associated with about 95% mortality over 3 to 4 days at 16 to 18°C among experimentally exposed veligers (Hine et al. 1998).

Diagnostic techniques

The virus is easier to detect in moribund animals than in apparently healthy animals. Also, young stages of oysters including larvae, spat and juveniles, seem to be more susceptible to the infection.

Gross observations

Pale digestive gland in spat and older oysters. Infected larvae stop feeding, swimming and exhibit velar lesions (less extended velum and detached parts of the velum are observed free in the water). Usually significant mortalities occur 6 days after spawning with peak mortalities (80 to 100%) between day 8 and 12 often during the summer time (Hine et al. 1992, Nicolas et al. 1992, Garcia et al. 2011, Schikorski et al. 2011b, Arzul et al. 2017).

Wet mounts

Larval velum cells are hypertrophied and detached from the tissue. Schikorski et al. (2011a) developed a protocol for the maintenance of infective OsHV-1 virus which involved the preparation of filtered (0.22 μm) tissue homogenates stored at 4°C for one month. They indicated that this preparation could be useful for studies concerning the transmission and the development of OsHV-1 infection.

Histology

Presumptive diagnosis can be made on the histological observations of intranuclear inclusion bodies that are eosinophilic, Feulgen positive and referred to as Cowdry type A nuclear inclusions, abnormal chromatin pattern (usually emarginated) and hypertrophied (enlarged) nuclei in various cells of oysters (including interstitial cells, connective tissue cells or fibroblasts and epithelium) as tabulated by Hine et al. (1998). Cowdry type A nuclear inclusions were not observed in OsHV infected juvenile C. gigas in California (Burge et al. 2006). The main histological change in juvenile oysters is the presence of abnormal nuclei (enlarged nuclei associated with marginated chromatin in fibroblast-like cells and highly condensed nuclear chromatin in ovoid cells interpreted as haemocytes) throughout the connective tissue especially in the mantle, labial palps, gills and digestive gland (Arzul et al. 2017). In juveniles, infections were usually focal where fibroblastic-like cells exhibit abnormal cytoplasmic basophilia (Renault 2008b). Cellular abnormalities are not associated with massive haemocytic accumulations (Renault and Novoa 2004). Burge et al. (2007) reported that microscopic changes in connective tissue and digestive tubules are consistent with herpesvirus infections in juvenile C. gigas from the west coast of the USA including:

Similar morphological changes in the digestive tubule epithelium were reported by other authors (Arzul et al. 2017).

Electron microscopy

Herpes-like virogenesis begins in the nucleus of infected cells where empty capsids and nucleocapsids containing an electron-dense, toroidal or brick-shaped core are observed (Renault 2016). The virions pass through the nuclear membrane into the cytoplasm. Intracytoplasmic particles are similar to nuclear ones and sometimes have a trilaminar unit-membrane. They can be free in the cytoplasm or grouped within cytoplasmic vesicles. Enveloped particles (100–180 nm in diameter) are released at the cell surface or by cytolysis (Arzul et al. 2017).

Infected C. gigas spat and larvae usually have virus particles in fibroblastic-like cells throughout connective tissues especially in mantle, labial palps, gills and digestive gland (Arzul et al. 2017). Because bivalve viruses have not been cultured, a confirmatory diagnosis is based on the following transmission electron microscopic features in infected cells from bivalves. Intranuclear inclusion bodies consisting of icosahedral (6- and 5-sided particles) virions 70-120 nm in diameter, a single coat and, occasionally, a dense nucleoid (or toroidal core). In C. gigas larvae, viral particles (capsid size of 72-97 nm) occur in the nuclei and occasionally in the cytoplasm of connective tissue cells of the velum, adductor muscle tissue and digestive gland (Renault 2011, Schikorski et al. 2011a, Burge and Friedman 2012, Hwang et al. 2013). Extracellular enveloped virons measure between 100 to 180 nm in diameter (Renault 2006, 2008b). The C. gigas viruses are most similar to the Betaherpesvirinae according to Hine et al. (1992) but are antigenically cross-reactive with channel catfish virus, which belongs to the Alphaherpesvirinae according to Le Deuff et al. (1995). Intranuclear particles 80 nm in diameter and enveloped cytoplasmic particles 160 to 180 nm in diameter occurred in infiltrating cells with enlarged nuclei (tentatively identified as haemocytes and fibroblasts) in the digestive gland of O. edulis (Comps and Cochennec 1993). A tailed envelope extensions (250-350 nm) has been reported on cytoplasmic mature viral particles found in some of the oyster species but not others. Hine et al. (1998), Renault and Novoa (2004) and Davison et al. (2005) presented morphological comparison of herpes-like viruses described from various species of oysters and comparison to other herpesviruses. Renault (2008b) indicated that larvae exhibit generalized infections with velar and mantle lesions, whereas focal infections usually occur in juveniles.

Immunological assay

An immunochemistry analysis using polyclonal antibodies was conducted on 7 µm tissue sections as described by Arzul et al. (2002).

DNA probes

DNA has been extracted from virions purified from fresh, heavily infected C. gigas larvae (Le Deuff and Renault 1999, Renault 2006) and the total genome of the virus (207439 base pairs) was completely sequenced (GenBank number AY509253). Sequence data demonstrate that the Ostreid Herpesvirus type 1 (OsHV-1) is not closely related to herpesviruses from vertebrate hosts (including fish) (Renault and Novoa 2004, Davison et al. 2005, Renault 2008a, Davison 2010, Burioli et al. 2017). The OsHV-1 genes are unspliced whereas those in herpesviruses of mammals and birds contain 1 interon and fish and amphibians contain 2 interons (Renault 2008b). Polymerase Chain Reaction (PCR) and in situ hybridisation (ISH) procedures have been developed for the detection of herpes-like viruses of oysters in France (Renault and Lipart 1998; Renault et al. 2000b; Renault and Arzul 2001; Arzul et al. 2002; Lipart and Renault 2002; Renault and Novoa 2004; Renault 2008a, b; Pepin et al. 2008; Martenot et al. 2010; Corbeil et al. 2015; Segarra et al. 2016; Renault 2016), in New Zealand (Webb et al. 2007) and on the west coast of the USA (Burge and Friedman 2012). Garcia et al. (2011) suggested 2 measures for improving the molecular detection of OsVH-1 during oyster mortality outbreaks:

A further complication is the lack of sensitivity of OsHV-1 DNA PCR assays for detecting latent infection or asymptomatic carriers of the disease. Thus, latently infected oysters, that are able to transmit the infection, are not always detected by PCR, limiting the value of PCR as a method to control movement of infected oysters. (EFSA (AHAW) 2015).

Arzul et al. (2017) indicated other major concerns that could hampered the routine use of molecular based diagnosis tools. “Not all regions of viral DNA are equally useful as targets for molecular detection. The assays often have not been thoroughly tested for inclusivity (detection of all types of the pathogen) or specificity (cross reaction with any other organism). The main concern is that molecular tools too often are developed from a few sequences without a good understanding of the overall sequence variability within the species. Moreover, molecular tools detect DNA and not necessarily a viable pathogen.”

Renault et al. (2004) developed an internal standard for OsHV-1 detection by PCR using a competitive PCR method in order to detect PCR inhibitors in oyster tissues, to validate sample preparation methods for PCR analysis and to quantify OsHV-1 DNA. Vigneron et al. (2004) indicated that PCR could be used to successfully amplify OsHV-1 DNA in samples of natural seawater water. Barbosa-Solomieu et al. (2004) adapted existing DNA extraction protocols and designed specific primers targeting small fragments (less than 200 bp) in order to detect OsHV-1 in fixed paraffin-embedded archival samples using PCR and ISH. Batista et al. (2005) developed a simple and rapid method of DNA extraction from oyster larvae for the detection of OsHV-1 by PCR. A critical review of the above procedures was published (Batista et al. 2007) and the European Food Safety Authority published a document that tabulated PCR detection methods (EFSA (AHAW) 2010). Pepin et al. (2008, and see Pepin 2013) developed a real-time PCR (quantitative PCR (qPCR)) assay for rapid, sensitive and quantitative detection of OsHV-1. Subsequently, this procedure was used by researchers to detect OsHV-1 in oysters under various experimental conditions in order to understand the epizootiology (Sauvage et al. 2009; Schikorski et al. 2011b; Clegg et al. 2014; Dégremont 2013; Renault et al. 2014a; Petton et al. 2015a, b; Segarra et al. 2016). Although, Dundon et al. (2011) showed that single conventional PCR (using the CF/CR primer pair) was more sensitive than real-time PCR, Pepin et al. (2008) and López-Sanmartín et al. (2016c) were unable to detect OsHV-1 DNA by conventional PCR but real-time PCR gave positive results. They determined that the differences in the detection of OsHV-1 DNA using the 2 PCR approaches was mainly attributed to the higher sensitivity of real time PCR methods when the intensity of infection is low (Pepin et al. 2008, López-Sanmartín et al. 2016c). Ren et al. (2010) developed a loop-mediated isothermal amplification (LAMP) assay for rapid, specific and sensitive detection of OsHV-1 DNA.

Martenot et al. (2010) described an alternative real-time PCR protocol based on TaqMan® chemistry, which they claimed was an improvement on the reference protocol of Pepin et al. (2008) in terms of sensitivity, specificity and rapidity (<3 h). This assay was used by several researchers including:

Burge et al. (2011) developed a SYBR® Green qPCR based on the A-region of the OsHV-1 genome. Various other primers (probes) and PCR assay variations have been used to detect OsHV-1 and its variants (Renault et al. 2012, Jenkins et al. 2013, Lynch et al. 2013, Martenot et al. 2013).

Sequencing of the PCR products obtained by amplification with primers C2-C6 (described by Renault and Arzul 2001) can be used to identify the OsHV-1 μVar strain definitively (Segarra et al. 2010; Martenot et al. 2011; Lynch et al. 2012, 2013; Jenkins et al. 2013; Burioli et al. 2017). The European Union Commission published a regulation that described a PCR assay using another primer pair (the CF-CR primers) that could be used to distinguish OsHV-1 and the variant OsHV-1 μVar based on the different mobility of the amplified products in agarose gel (EU Commission Regulation 175/2010). However, Aranguren et al. (2012) indicated that differentiation based on this assay was not conclusive and could lead to an erroneous interpretation, especially when co-infection of 2 genotypes occurred in the same sample, because there is only a difference of 16 bp between the 2 strains (i.e., the primers CF/CR, amplified 157 bp of OsHV-1 μVar and 173 bp of OsHV-1). Thus, they proposed a specific polymerase chain reaction - restriction fragment length polymorphism (PCR-RFLP) assay using the MfeI restriction enzyme to identify OsHV-1 μVar and distinguish it from the reference OsHV-1 genotype (Aranguren et al. 2012). Renault et al. (2014b) developed a genotyping method to characterise clinical OsHV-1 specimens by targeting a particular microsatellite locus located in the ORF4 area which allowed accurate discrimination to detect OsHV-1 polymorphism. Batista et al. (2015) suggested that a non-coding region (NC1/NC2 region) located between ORFs 49 and 50 may be a highly polymorphic region and hence of particular interest for molecular epidemiological studies. However, Arzul et al. (2017) indicated that ORF100 (DNA polymerase) appeared less polymorphic. Segarra et al. (2014b) suggested that an OsHV-1-specific reverse transcriptase real time PCR targeting 39 viral genes may be a new tool for diagnosis and could be used to complement viral DNA detection in order to monitor viral replication thereby assessing the viral cycle and infection status. Nevertheless, the PCR assay chosen for surveillance must be validated for all components of the assay and as indicated by Lynch et al. (2013), further validation of a reliable and sensitive PCR method should include an interlaboratory comparison using a range of diagnostic techniques and tissue types.

In situ hybridization (ISH) procedures often use digoxigenin (DIG)-labelled probe to detect OsHV-1 DNA in formalin-fixed, paraffin-embedded oyster tissues (Arzul et al. 2017). This assay indicated that OsHV-1 occurred in the connective tissues of C. gigas spat as identified previously using light and transmission electron microscopy as well as in the visceral ganglion of the oyster nervous system (Renault and Lipart 1998, Lipart and Renault 2002). Infected organs included gills, labial palps, mantle, digestive gland, heart, adductor muscle, and gonads (Lipart and Renault 2002, Batista et al. 2014, Segarra et al. 2016). Segarra et al. (2016) also used ISH to detect RNA of OsHV-1 in tissues of C. gigas spat. Application of PCR, ISH, and immunochemistry suggested that herpes-like virus occurred in a high prevalence (>75%) of apparently normal C. gigas adults and the presence of viral DNA and viral proteins in the gonad supported the hypothesis of vertical transmission from adults to larvae (Arzul et al. 2002). However, the detection of viral DNA in parental oysters did not systematically correspond to infection or result in successful transmission to the progeny although the infection status of the parents appeared to influence infection and survival rates of the progeny (Renault and Novoa 2004). Corbeil et al. (2015) and López-Sanmartín et al. (2016b) presented methods to detect OsHV-1 transcripts in infected C. gigas and O. edulis, respectively, using ISH.

Methods of control

The European Food Safety Authority panel on Animal Health and Welfare (EFSA (AHAW) 2010) determined that risk factors associated with the severe mortality events in cultured juvenile C. gigas in the summers of 2008 and 2009 in the main European producing countries included an increase or a sudden change in the temperature, and husbandry practices such as introduction of non-certified possibly infected spat, movements and mixing of populations and age groups. The panel concluded that it is not safe to transfer oysters older than 18 months from affected areas to areas not affected. Once infected, an area is not likely to regain freedom from OsHV-1 if a wild population of C. gigas is present (EFSA (AHAW) 2015). They recommended that to promote and preserve a high health status and in particular to prevent and/or control "increased mortality", measures are urgently needed to improve the general level of biosecurity in the oyster aquaculture industry in Europe. Furthermore, to minimize the risk of subsequent transfer of infectious agents from hatcheries and wild-caught spat, there is a need to establish the health status of oyster spat at source. An assessment of the health status should include results of regular batch laboratory testing (at least in regards to OsHV-1 reference strain and OsHV-1 μVar) and epidemiological assessment. Improved diagnostic methods should be developed and clear criteria for viral strain differentiation taking in account genotype and epidemiological criteria are necessary (EFSA (AHAW) 2010). This approach was reiterated by Coen and Bishop (2015) who emphasized the importance of using newly emerging molecular tools and remote sensing techniques to study molluscan diseases. Also, the compilation and analysis of molecular data from around the world by Mineur et al. (2015), resulting in an inference that the geographical origin of OsHV-1 was Asian, highlights the risks of European stock improvements, by means of overseas shellfish imports. Pernet et al. (2016) concluded that reconsidering the key issues of disease management by incorporating multidisciplinary science could provide a holistic understanding of OsHV-1 and increase the benefit of research to policymakers.

Renault (2016) stated that rapid and accurate differential diagnosis based on molecular techniques is the key to success in controlling OsHV-1 infection outbreaks. Oden et al. (2011) indicated that molecular monitoring of viral load should be a particularly useful tool for preventing mortality by enabling oyster farmers to evaluate risks before batch transfers or before setting oysters out in the sea. They established that a viral load threshold of 4.4×105 copies of OsVH-1 DNA in 50 mg of C. gigas tissue appeared to be useful to oyster farmers for this purpose (Oden et al. 2011). Lynch et al. (2013) confirmed that rapid, reliable, and highly sensitive diagnostic techniques are necessary for the effective control and management of disease in aquaculture. Normand et al. (2014) discussed the use of detection methods in relation to early rearing practices and disease control strategies. In Australia, the management of OsHV-1 mainly involves active surveillance, rigorous biosecurity protocols and mollusc breeding programs targeting production of resistant animals (Paul-Pont et al. 2013a). Pande et al. (2015) proposed a survey design methodology that used hydrodynamically-modelled epidemiological units (based on groups of animals sharing a similar risk) that could help inform management decisions. Gustafson et al. (2021) presented expert guidance for OsHV-1 surveillance design and system sensitivity calculation for optimizing surveillance for early disease detection.

Moving oysters into cooler waters may reduce the pathogenicity of the virus. The case in Maine, U.S.A. was reported following transfer of oysters to thermal effluent from a power station, for grow-out. Some cases in New Zealand, France and California occurred in mid-summer at a time of elevated water temperatures. Le Deuff et al. (1996) reported 80 to 90 % mortality in C. gigas larvae reared at 25 to 26°C but not in larvae reared at 22 to 23°C. However, morbidity and mortality can occur below temperatures at which viral replication is completed and latent infections will persist. Using laboratory studies, Hick et al. (2016) determined that OsHV-1 remained infectious in seawater for 2 days at 20°C and in wet or dry, non-living C. gigas tissues for at least 7 days at 20°C. Also using laboratory studies, Pernet et al. (2015) found that OsHV-1 persists in C. gigas even at low temperatures (10 and 13°C) and was reactivated during subsequent thermal elevation to 21°C. Thus, low temperature treatments did not improve overall survival of oyster seed infected with OsHV-1 suggesting that moving infected oysters to a cooler area would only delays mortality and may increase the risk of infection in neighbouring stocks when rising temperatures become permissive for viral replication (Pernet et al. 2015). However, Petton et al. (2013) determined that oysters previously infected with OsHV-1 could recover after being kept at 13.0°C for 40 days and therefore suggested that long-term holding at low temperatures may offer a way to mitigate oyster mortalities. In addition, de Kantzow et al. (2018, 2019 a, b, 2020) indicated that juvenile C. gigas that were pre-exposed to OsHV-1 at 18°C had improved survival when subsequently exposed at 22°C. In O. chilensis, the opposite appeared to occur because the virus was observed to replicate at ambient temperatures (16° to 18°C) but not at higher temperatures (Hine et al. 1998). Results of experimental transmission studies using infected C. gigas larvae indicate that the virus remained infectious after several months of storage at -20°C (Le Deuff et al. 1994).

For areas in which the virus is not enzootic, the most sensible management is to prevent its introduction with contaminated broodstock, larvae or seed (juveniles for grow-out). When OsHV-1 is first detected in a new environment, de Kantzow et al. (2017) indicated that for the development of effective disease control measures it is important to describe the impact of OsHV-1 in the new environment and identifying the association between farm management and mortality. In Enzootic areas, mortality related to OsHV-1 in hatchery-produced oysters can be avoided using ponds or tanks because these oysters can be protected from exposure to OsHV-1, (Degremont and Benabdelmouna 2014). Results of experiments conducted by Whittington et al. (2015a) supported the hypothesis that OsHV-1 is carried on particles rather than being uniformly distributed in water. Thus, the removal of the putative particulate vector of OsHV-1 from seawater using aging/sedimentation of water or filtration to 5 μm enabled C. gigas spat to survive despite the presence of OsHV-1 μVar in the water supply (Whittington et al. 2015a). Although the results of Evans et al. (2016) were consistent with the hypothesis that OsHV-1 may be attached to particles, they determined that it may not be possible to remove OsHV-1 completely from the seawater of a recirculation system during a disease event using biofiltration and ultra-violet light (40W—65LMP/3900LPH at 30mJ/cm2 (90% UVT) 40 mm connections) irradiation alone. After exploring the first interactions between OsHV-1 and C. gigas cells, Martenot et al. (2019) determined that 30 µg/ml of dextran sulfate significantly reduced spat mortality rates in experimental conditions and suggested that such new approaches may help control OsHV-1 in confined facilities.

Hick et al. (2016) indicated that OsHV-1 was inactivated by:

Sodium hypochlorite (50 ppm available chlorine for 15 min) inactivated OsHV-1 in relatively clean seawater, but this treatment was not effective after addition of protein (10% v/v foetal bovine serum) and a concentration of 200 ppm available chlorine for 15 min did not inactivate OsHV-1 in oyster tissue (Hick et al. 2016).

Clegg et al. (2014) considered a range of risk factors relating to farm management but none were found significantly related to mortalities associated with OsVH-1 μVar. However, Dégremont (2013) and Azema et al. (2015b) indicated that larger juvenile C. gigas in a cohort always tended to be more resistant to OsHV-1 than smaller ones. Prudent management strategies for oyster growers such as deploying juveniles at a site favouring the growth of oysters after the threat of exposure to OsHV-1 has passed (i.e. at the end of the risk period when seawater temperatures return to less than 16°C), and by using cultural practices favouring high growth and/or a site for which the risk period is short due to the seawater temperature could potentially offer viable solutions for disease control (Dégremont 2013, Carrasco et al. 2017). Additional mitigation strategies include the regulation of oyster movements between sites, spatial planning, and taking into account seed origin (Petton et al. 2015b). In Australia, Whittington et al. (2015b) confirmed that cumulative mortality for adult C. gigas attributed to OsHV-1 can be reduced by cultivation at a high height in the inter-tidal zone during the summer risk period for OsHV-1 infection. However, the final cumulative mortalities for C. gigas spat were high regardless of the tidal height indicating that other mitigation strategies need to be developed for young oysters (Whittington et al. 2015b). Oliver et al. (2019) reported that 6 month old C. gigas pre-exposed to air for 24 h prior to OsHV-1 challenge by cohabitation were more resilient to infection, but this result needs to be validated in the field and more complex confounding factors need to be considered. Abollo Rodrígues and Villalba García (2013) published, on the internet, a document that describes the disease and recommended methods of control. Nevertheless, following the qualitative analysis of mortality data obtained from experimental populations of C. gigas during natural epizootics of OsHV-1 disease in Australia, Whittington et al. (2018) suggested that prevention and control of OsHV-1 in C. gigas will require multiple interventions.

Based on the high genetic basis underlying the variance of resistance of C. gigas to the prevalence and intensity of infection and resulting mortality, Sauvage et al. (2009, 2010), Green et al. (2015a), Dégremont et al. (2015a, b, 2016a), Renault (2016) and Divilov et al. (2019) suggested that there might be a possibility to improve resistance to OsHV-1 by selective breeding. Segarra et al. (2014c) and Azema et al. (2015a, b, c) confirmed that susceptibility to OsHV-1 infection has a significant genetic component resulting in divergent responses of C. gigas families in terms of mortality. Dégremont (2011, 2013) reported that juvenile (6 month old) C. gigas selected for resistance to "summer mortality" (mainly attributed to OsHV-1 during the study) had a significant resistance to mortality (only 5% mortality) when compared to a control batch (53% mortality) and a batch descended from one family selected to be susceptible to the summer mortality phenomenon (94% mortality). Fleury and Huvet (2012) also reported high heritability for resistance to "summer mortality" in C. gigas and developed lines of oysters resistant to this disease. Dégremont et al. (2016b) determined that difference in mortality or the delayed on set of mortality between larvae from selected and unselected C. gigas broodstock indicate larvae from selected broodstock have a genetic resistance to OsHV-1 infection. However, Azéma et al. (2016) indicated that C. gigas exposed to both OsHV-1 and the oyster pathogenic bacteria Vibrio aestuarians could experience dramatic mortality rates, even in oysters selected for their higher resistance to OsHV-1, represents an important threat for oyster farmers. Nevertheless, the selection for dual resistance to OsHV-1 and V. aestuarianus infection in C. gigas might reduce the impact of these 2 major diseases by selecting families that have the highest breeding values for resistance to both diseases (Azema et al. 2017). Camara et al. (2017) indicated that the laboratory virus challenge is a simple and relatively effective tool for selecting breeding specifically towards OsHV-1 resistance or as part of a controlled multi-trait program. Gutierrez et al. (2018) used a genome-wide association study for C. gigas resistance to OsHV, and suggested that this approach would enhance selective breeding for disease resistance in farmed oysters. In addition, Agnew et al. (2020) emphasized the need to consider resistance to infection in addition to survival as traits in breeding programs to reduce the risk of the spread of OsHV-1 variants.

Apparently, triploidy in C. gigas confers neither advantage nor disadvantage in survival after challenge with OsHV-1 and resistance to OsHV-1 was not substantially altered by triploidization (Dégremont et al. 2015b, 2016a). The genes induced in C. gigas haemocytes challenged with OsHV-1 that were identified by Renault et al. (2011) may serve as markers of interest in breeding programs to obtain selected oysters presenting OsHV-1 resistance. Green et al. (2014b) suggested that cavortin, a multifunctional protein involved in immunity might be useful for marker-assisted selection of disease resistant oysters. Dégremont et al. (2015c) indicated that after four generations C. gigas subjected to mass selection under field conditions for their higher resistance to OsHV-1 infection showed higher growth (58.4 mm – 19.4 g) than controls (51.4 mm – 15.2 g), and had significantly improved yield (13.3 kg for the selected oysters over 1.2 kg for the controls). Green and Montagnani (2013) and Green et al. (2014a, 2015c) published evidence that injection with synthetic double stranded RNA (specifically, a nucleic acid named poly(I:C)) activates an innate immune response (i.e., immune priming) in C. gigas that provides protection against OsHV-1 infection. Lafont et al. (2017, 2020) demonstrated that this phenomenon persisted for at least 5 months in C. gigas but failed to protect oysters against a pathogenic bacteria (Vibrio tasmaniensis Strain LGP32) and thus suggested the production of a specific antiviral response. Green et al. (2016b), Green and Speck (2018) and Lafont et al. (2019) determined that female oyster broodstock treated with poly(I:C) produce offspring (D-veliger larvae) with enhanced protection against OsHV-1 infection. This process, broadly defined as trans-generational immune priming (TGIP) is the phenomenon by which a parent can transfer immunological information based on previous infections in the form of protection to its offspring, was reviewed by Agius et al. (2020). However, Robinson and Green (2020) found that C. gigas larvae produced from maternal immune priming were smaller, and had higher total bacteria and Vibrio loads compared to control larvae and suggested that improved offspring survival to OsHV-1 was a potentially traded off with other important life history traits, such as larval growth rate and destabilisation of the microbiome.

References

Abbadi, M., G. Zamperin, M. Gastaldelli, F. Pascoli, U. Rosani, A. Milani, A. Schivo, E. Rossetti, E. Turolla, L. Gennari, A. Toffan, G. Arcangeli and P. Venier. 2018. Identification of a newly described OsHV-1 µvar from the North Adriatic Sea (Italy). Journal of General Virology 99: 693-703.

Abollo Rodríguez, E. and A. Villalba García. 2013. Guía de autocontrol virus herpes de ostreidos. Internet publication with open access. (in French only)

Agius, J.R., S. Corbeil and K.J. Helbig. 2020. Immune control of herpesvirus infection in molluscs. Pathogens 9(8): 618, 11 pp.

Agnew, M.V., C.S. Friedman, C. Langdon, K. Divilov, B. Schoolfield, B. Morga, L. Dégremont, A.K. Dhar, P. Kirkland, B. Dumbauld and C.A. Burge. 2020. Differential mortality and high viral load in naive Pacific oyster families exposed to OsHV-1 suggests tolerance rather than resistance to infection. Pathogens 9(12): 1057,18 pp.

Allam, B. and D. Raftos. 2015. Immune responses to infectious diseases in bivalves. Journal of Invertebrate Pathology 131: 121-136.

Alfjorden, A., M. Areskog, D. Bruno, R. Carnegie, D. Cheslett, S. Feist, S. Ford, S. Jones, A. Lillehaug, L. Madsen, T. Renault, N. Ruane and P. Vennerström. 2017. New Trends in Important Diseases Affecting the Culture of Fish and Molluscs in the ICES Area 2002 – 2015. In ICES Cooperative Research Report No. 337. Anderson, E.D., N. Ruane, R. Carnegie, eds. (Copenhagen, Denmark, International Council for the Exploration of the Sea, Conseil International pour l'Exploration de la Mer). 50 pp.

Aranguren, R., M.M. Costa, B. Novoa and A. Figueras. 2012. First detection of herpesvirus variant (OsHV-1μvar) in Pacific oysters (Crassostrea gigas) in Spain and development of a rapid method for its differential diagnosis. Bulletin of the European Association of Fish Pathologists 32: 24-29.

Arzul, I., T. Renault, C. Lipart and A.J. Davison. 2001a. Evidence for interspecies transmission of oyster herpesvirus in marine bivalves. Journal of General Virology 82: 865-870.

Arzul, I., T. Renault and C. Lipart. 2001b. Experimental herpes-like viral infections in marine bivalves: demonstration of interspecies transmission. Diseases of Aquatic Organisms 46: 1-6.

Arzul, I., J.-L. Nicolas, A.J. Davison and T. Renault. 2001c. French scallops: a new host for ostreid herpesvirus-1. Virology 290: 342-349.

Arzul, I., T. Renault, A. Thébault and A. Gérard. 2002. Detection of oyster herpesvirus DNA and proteins in asymptomatic Crassostrea gigas adults. Virus Research 84: 151-160.

Arzul, I., S. Corbeil, B. Morga and T. Renault. 2017. Viruses infecting marine molluscs. Journal of Invertebrate Pathology 147: 118-135.

Azema, P., M.-A. Travers, J.-B. Lamy and L. Dégremont. 2015a. Genetic parameters for OsHV-1 and Vibrio aestuarianus resistance in Crassostrea gigas: First results using controlled challenges. Journal of Shellfish Research 34: 606-607. (Abstract).

Azema, P., M.-A. Travers and L. Dégremont. 2015b. Genotype by size interaction for OsHV-1 resistance in Crassostrea gigas. Journal of Shellfish Research 34: 607. (Abstract).

Azéma, P., M.-A. Travers, J. De Lorgeril, D. Tourbiez and L. Dégremont. 2015. Can selection for resistance to OsHV-1 infection modify susceptibility to Vibrio aestuarianus infection in Crassostrea gigas? First insights from experimental challenges using primary and successive exposures. Veterinary Research 46: 139, 14 pp.

Azéma, P., M.-A. Travers, A. Benabdelmouna and L. Dégremont. 2016. Single or dual experimental infections with Vibrio aestuarianus and OsHV-1 in diploid and triploid Crassostrea gigas at the spat, juvenile and adult stages. Journal of Invertebrate Pathology 139: 92-101.

Azéma, P., J.-B. Lamy, P. Boudry, T. Renault, M.-A. Travers and L. Dégremont. 2017. Genetic parameters of resistance to Vibrio aestuarianus, and OsHV-1 infections in the Pacific oyster, Crassostrea gigas, at three different life stages. Genetics Selection Evolution 49: 23, 16 pp.

Bai, C., C. Wang, J. Xia, H. Sun, S. Zhang and J. Huang. 2015. Emerging and endemic types of Ostreid herpesvirus 1 were detected in bivalves in China. Journal of Invertebrate Pathology 124: 98-106.

Barbieri, E.S., C.D. Medina, N. Vázquez, C. Fiorito, A. Martelli, A. Wigdorovitz, E. Schwindt, B. Morga, T. Renault, V. Parreño and P.J. Barón. 2019. First detection of Ostreid herpesvirus 1 in wild Crassostrea gigas in Argentina. Journal of Invertebrate Pathology 166: 107222, 6 pp.

Barbosa-Solomieu, V., L. Miossec, R. Vázquez-Juárez, F. Ascencio-Valle and T. Renault. 2004. Diagnosis of Ostreid herpesvirus 1 in fixed paraffin-embedded archival samples using PCR and in situ hybridisation. Journal of Virological Methods 119: 65-72.

Barbosa-Solomieu, V., L. Dégremont, R. Vázquez-Juárez, F. Ascencio-Valle, P. Boudry and T. Renault. 2005. Ostreid Herpesvirus 1 (OsHV-1) detection among three successive generations of Pacific oysters (Crassostrea gigas). Virus Research 107: 47-56.

Barbosa Solomieu, V., T. Renault and M.-A. Travers. 2015. Mass mortality in bivalves and the intricate case of the Pacific oyster, Crassostrea gigas. Journal of Invertebrate Pathology 131: 2-10.

Batista, F.M., N. Taris, P. Boudry and T. Renault. 2005. Detection of ostreid herpesvirus-1 (OsHV-1) by PCR using a rapid and simple method of DNA extraction from oyster larvae. Diseases of Aquatic Organisms 64: 1-4.

Batista, F., I. Arzul, J.-F. Pepin, F. Ruano, C.S. Friedman, P. Boudry and T. Renault. 2007. Detection of ostreid herpesvirus 1 DNA by PCR in bivalve molluscs: A critical review. Journal of Virological Methods 139: 1-11.

Batista, F., M. López-Sanmartín, P. Boudry, J.I. Navas, F. Ruano, T. Renault, V.G. Fonseca and A. Leitão. 2014. Insights on the association between somatic aneuploidy and ostreid herpesvirus 1 detection in the oysters Crassostrea gigas, C. angulata and their F1 hybrids. Aquaculture Research 47: 1530-1536.

Batista, F.M., M. López-Sanmartín, A. Grade, I. Morgado, M. Valente, J.I. Navas, D.M. Power and F. Ruano. 2015. Sequence variation in ostreid herpesvirus 1 microvar isolates detected in dying and asymptomatic Crassostrea angulata adults in the Iberian Peninsula: Insights into viral origin and spread. Aquaculture 435: 43-51.

Burge, C.A. 2010. Examining the Roles of Environment, Host, and Pathogen in the Host-Pathogen Relationship Between the Oyster Herpesvirus and the Pacific Oyster. Doctoral dissertation. University of Washington.

Burge, C.A. and C.S. Friedman. 2012. Quantifying Ostreid herpesvirus (OsHV-1) genome copies and expression during transmission. Microbial Ecology 63: 596-604.

Burge, C.A., F.J. Griffin and C.S. Friedman. 2006. Mortality and herpesvirus infections of the Pacific oyster Crassostrea gigas in Tomales Bay, California, USA. Diseases of Aquatic Organisms 72: 31-43.

Burge, C.A., L.R. Judah, L.L. Conquest, F.J. Griffin, D.P. Cheney, A. Suhrbier, B. Vadopalas, P.G. Olin, T. Renault and C.S. Friedman. 2007. Summer seed mortality of the Pacific oyster, Crassostrea gigas Thunberg grown in Tomales Bay, California, USA: the influence of oyster stock, planting time, pathogens, and environmental stressors. Journal of Shellfish Research 26: 163-172.

Burge, C.A., R.E. Strenge and C.S. Friedman. 2011. Detection of the oyster herpesvirus in commercial bivalves in northern California, USA: conventional and quantitative PCR. Diseases of Aquatic Organisms 94: 107-116.

Burge, C.A., K.S. Reece, A.K. Dhar, P. Kirkland, B. Morga, L. Dégremont, N. Faury, B.J.T. Wippel, A. MacIntyre and C.S. Friedman. 2020. First comparison of French and Australian OsHV-1 µvars by bath exposure. Diseases of Aquatic Organisms 138: 137-144.

Burioli, E.A.V., M. Prearo and M. Houssin. 2017. Complete genome sequence of Ostreid herpesvirus type 1 µVar isolated during mortality events in the Pacific oyster Crassostrea gigas in France and Ireland. Virology 509: 239-251.

Camara, M.D., S. Yen, H.F. Kaspar, A. Kesarcodi-Watson, N. King, A.G. Jeffs and L.A. Tremblay. 2017. Assessment of heat shock and laboratory virus challenges to selectively breed for ostreid herpesvirus 1 (OsHV-1) resistance in the Pacific oyster, Crassostrea gigas. Aquaculture 469: 50-58.

Carnegie, R.B. 2011. Update on emerging disease outbreaks in Europe, New Zealand, and Australia, and relevance to US east coast shellfish interests. Journal of Shellfish Research 30: 445. (Abstract).

Carrasco, N., I. Gairin, J. Pérez, K.B. Andree, A. Roque, M. Fernández-Tejedor, C.J. Rodgers, C. Aguilera and M.D. Furones. 2017. A production calendar based on water temperature, spat size, and husbandry practices reduce OsHV-1 µvar impact on cultured Pacific oyster Crassostrea gigas in the Ebro Delta (Catalonia), Mediterranean coast of Spain. Frontiers in Physiology 8: 125, 10 pp.

Clegg, T.A., T. Morrissey, F. Geoghegan, S.W. Martin, K. Lyons, S. Ashe and S.J. More. 2014. Risk factors associated with increased mortality of farmed Pacific oysters in Ireland during 2011. Preventive Veterinary Medicine 113: 257-267.

Comps, M. and N. Cochennec. 1993. A Herpes -like virus from the European oyster Ostrea edulis L. Journal of Invertebrate Pathology 62: 201-203.

Coen, L.D. and M.J. Bishop. 2015. The ecology, evolution, impacts and management of host–parasite interactions of marine molluscs. Journal of Invertebrate Pathology 131: 177-211.

Corbeil, S., N. Faury, A. Segarra and T. Renault. 2015. Development of an in situ hybridization assay for the detection of ostreid herpesvirus type 1 mRNAs in the Pacific oyster, Crassostrea gigas. Journal of Virological Methods 211: 43-50.

Corporeau, C., D. Tamayo, F. Pernet, C. Quéré and S. Madec. 2014. Proteomic signatures of the oyster metabolic response to herpesvirus OsHV-1 μVar infection. Journal of Proteomics 109: 176-187.

da Silva, P.M., T. Renault, J. Fuentes and A. Villalba. 2008. Herpesvirus infection in European flat oysters Ostrea edulis obtained from brood stocks of various geographic origins and grown in Galicia (NW Spain). Diseases of Aquatic Organisms 78: 181-188.

Davison, A.J., B.L. Trus, N. Cheng, A.C. Steven, M.S. Watson, C. Cunningham, R.M. Le Deuff and T. Renault. 2005. A novel class of herpervirus with bivalve hosts. Journal of General Virology 86: 41-53.

Davison, A.J. 2010. Herpesvirus systematics. Veterinary Microbiology 143: 52-69.

Dégremont, L. 2011. Evidence of herpesvirus (OsHV-1) resistance in juvenile Crassostrea gigas selected for high resistance to the summer mortality phenomenon. Aquaculture 317: 94-98.

Dégremont, L. 2013. Size and genotype affect resistance to mortality caused by OsHV-1 in Crassostrea gigas. Aquaculture 416–417: 129-134.

Degremont, L. and A. Benabdelmouna. 2014. Mortality associated with OsHV-1 in spat Crassostrea gigas: role of wild-caught spat in the horizontal transmission of the disease. Aquaculture International 22: 1767-1781.

Dégremont, L., J.-B. Lamy, J.-F. Pepin, M.-A. Travers and T. Renault. 2015a. New Insight for the genetic evaluation of resistance to ostreid herpesvirus infection, a worldwide disease, in Crassostrea gigas. PLoS ONE 10(6): e0127917, 12 pp.

Dégremont, L., C. Garcia and S.K.J. Allen. 2015b. Genetic improvement for disease resistance in oysters: A review. Journal of Invertebrate Pathology 131: 226-241.

Dégremont, L., M. Nourry and E. Maurouard. 2015c. Mass selection for survival and resistance to OsHV-1 infection in Crassostrea gigas spat in field conditions: response to selection after four generations. Aquaculture 446: 111-121.

Dégremont, L., C. Ledu, E. Maurouard, M. Nourry and A. Benabdelmouna. 2016a. Effect of ploidy on the mortality of Crassostrea gigas spat caused by OsHV-1 in France using unselected and selected OsHV-1 resistant oysters. Aquaculture Research 47: 777-786.

Dégremont, L., B. Morga, S. Trancart and J.-F. Pépin. 2016b. Resistance to OsHV-1 infection in Crassostrea gigas larvae. Frontiers in Marine Science 3: 15, 12 pp.

de Kantzow, M.C. 2020. Epidemiological investigations inform Ostreid herpesvirus 1 disease control in Pacific oysters (Crassostrea gigas). Doctor of Philosophy. Faculty of Science, Sydney Institute of Veterinary Science, University of Sydney.

de Kantzow, M., P. Hick, J.A. Becker and R.J. Whittington. 2016. Effect of water temperature on mortality of Pacific oysters Crassostrea gigas associated with microvariant ostreid herpesvirus 1 (OsHV-1 µVar). Aquaculture Environment Interactions 8: 419-428.

de Kantzow, M.C., P.M. Hick, N.K. Dhand and R.J. Whittington. 2017. Risk factors for mortality during the first occurrence of Pacific Oyster Mortality Syndrome due to Ostreid herpesvirus – 1 in Tasmania, 2016. Aquaculture 468: 328-336.

de Kantzow, M.C., R.J. Whittington and P.M. Hick. 2018. Conditioning Pacific oyster (Crassostrea gigas) spat for improved survival of Ostreid Herpesvirus – 1 (Oshv-1) by controlled infection. In: 8th International Symposium on Aquatic Animal Health (Charlottetown, Prince Edward Island), Session Invertebrate and Shellfish Diseases 2.

de Kantzow, M.C., R.J. Whittington and P. Hick. 2019a. Prior exposure to Ostreid herpesvirus 1 (OsHV-1) at 18 °C is associated with improved survival of juvenile Pacific oysters (Crassostrea gigas) following challenge at 22 °C. Aquaculture 507: 443-450.

de Kantzow, M., R. Whittington and P. Hick. 2019b. Different in vivo growth of ostreid herpesvirus 1 at 18°C and 22°C alters mortality of Pacific oysters (Crassostrea gigas). Archives of Virology 164: 3035-3043.

Delisle, L., B. Petton, J.F. Burguin, B. Morga, C. Corporeau and F. Pernet. 2018. Temperature modulate disease susceptibility of the Pacific oyster Crassostrea gigas and virulence of the Ostreid herpesvirus type 1. Fish & Shellfish Immunology 80: 71-79.

de Lorgeril, J., A. Lucasson, B. Petton, E. Toulza, C. Montagnani, C. Clerissi, J. Vidal-Dupiol, C. Chaparro, R. Galinier, J.-M. Escoubas, P. Haffner, L. Dégremont, G.M. Charrière, M. Lafont, A. Delort, A. Vergnes, M. Chiarello, N. Faury, T. Rubio, M.A. Leroy, A. Pérignon, D. Régler, B. Morga, M. Alunno-Bruscia, P. Boudry, F. Le Roux, D. Destoumieux-Garzόn, Y. Gueguen and G. Mitta. 2018. Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nature Communications 9: 4215, 14 pp.

de Melo, C.M.R., E. Durland and C. Langdon. 2016. Improvements in desirable traits of the Pacific oyster, Crassostrea gigas, as a result of five generations of selection on the West Coast, USA. Aquaculture 460: 105-115.

Divilov, K., B. Schoolfield, B. Morga, L. Dégremont, C.A. Burge, D. Mancilla Cortez, C.S. Friedman, G.B. Fleener, B.R. Dumbauld and C. Langdon. 2019. First evaluation of resistance to both a California OsHV-1 variant and a French OsHV-1 microvariant in Pacific oysters.  BMC Genetics 20: 96, 9 pp.

Domeneghetti, S., L. Varotto, M. Civettini, U. Rosani, M. Stauder, T. Pretto, E. Pezzati, G. Arcangeli, E. Turolla, A. Pallavicini and P. Venier. 2014. Mortality occurrence and pathogen detection in Crassostrea gigas and Mytilus galloprovincialis close-growing in shallow waters (Goro lagoon, Italy). Fish & Shellfish Immunology 41: 37-44.

Dundon, W.G., I. Arzul, E. Omnes, M. Robert, C. Magnabosco, M. Zambon, L. Gennari, A. Toffan, C. Terregino, I. Capua and G. Arcangeli. 2011. Detection of Type 1 Ostreid Herpes variant (OsHV-1 μvar) with no associated mortality in French-origin Pacific cupped oyster Crassostrea gigas farmed in Italy. Aquaculture 314: 49-52.

Elston, R.A. 1993. Infectious diseases of the Pacific oyster, Crassostrea gigas. Annual Review of Fish Diseases 3: 259-276.

Elston, R. 1997. Special topic review: bivalve mollusc viruses. World Journal of Microbiology and Biotechnology 13: 393-403.

Elston, R.A. 1999. Health management, development and histology of seed oysters. Chapter 10. Herpes-like virus infection of larval and juvenile oysters. pp. 71-74. World Aquaculture Society, Baton Rouge, Louisiana, USA. 110 pp.

European Food Safety Authority (EFSA) Panel on Animal Health and Welfare (AHAW). 2010. Scientific opinion on the increased mortality events in Pacific oyster (Crassostrea gigas). EFSA Journal 8(11): 1894, 60 pp.

European Food Safety Authority (EFSA) Panel on Animal Health and Welfare (AHAW). 2015. Scientific opinion on oyster mortality. EFSA Journal 13(6): 4122, 59 pp.

EU Commission Regulation No 175/2010 of 2 March 2010 implementing Council Directive 2006/88/ EC as regards measures to control increased mortality in oysters of the species Crassostrea gigas in connection with the detection of Ostreid herpesvirus-1 μvar (OsHV-1 μvar).

Evans, O., I. Paul-Pont, P. Hick and R.J. Whittington. 2014. A simple centrifugation method for improving the detection of Ostreid herpesvirus-1 (OsHV-1) in natural seawater samples with an assessment of the potential for particulate attachment. Journal of Virological Methods 210: 59-66.

Evans, O., P. Hick, N. Dhand and R.J. Whittington. 2015. Transmission of Ostreid herpesvirus-1 in Crassostrea gigas by cohabitation: effects of food and number of infected donor oysters. Aquaculture Environment Interactions 7: 281-295.

Evans, O., P. Hick and R.J. Whittington. 2016. Distribution of Ostreid herpesvirus-1 (OsHV-1) microvariant in seawater in a recirculating aquaculture system. Aquaculture 458: 21-28.

Evans, O., P. Hick and R.J. Whittington. 2017a. Detection of Ostreid herpesvirus-1 microvariants in healthy Crassostrea gigas following disease events and their possible role as reservoirs of infection. Journal of Invertebrate Pathology 148: 20-33.

Evans, O., I. Paul-Pont and R.J. Whittington. 2017b. Detection of ostreid herpesvirus 1 microvariant DNA in aquatic invertebrate species, sediment and other samples collected from the Georges River estuary, New South Wales, Australia. Diseases of Aquatic Organisms 122: 247-255.

Farley, C.A. 1978. Viruses and viruslike lesions in marine mollusks. Marine Fisheries Review 40: 18-20.

Farley, C.A., W.G. Banfield, G. Kasnic Jr. and W.S. Foster. 1972. Oyster Herpes -type virus. Science 178 (4062): 759-760.

Fleury, E. and A. Huvet. 2012. Microarray analysis highlights immune response of Pacific oysters as a determinant of resistance to summer mortality. Marine Biotechnology 14: 203-217.

Friedman, C.S., R.M. Estes, N.A. Stokes, C.A. Burge, J.S. Hargrove, B.J. Barber, R.A. Elston, E.M. Burreson and K.S. Reece. 2005. Herpes virus in juvenile Pacific oysters Crassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes. Diseases of Aquatic Organisms 63: 33-41.

Fuhrmann, M., B. Petton, V. Quillien, N. Faury, B. Morga and F. Pernet. 2016. Salinity influences disease-induced mortality of the oyster Crassostrea gigas and infectivity of the ostreid herpesvirus 1 (OsHV-1). Aquaculture Environment Interactions 8: 543-552.

Fuhrmann, M., L. Delisle, B. Petton, C. Corporeau and F. Pernet. 2018. Metabolism of the Pacific oyster, Crassostrea gigas, is influenced by salinity and modulates survival to the Ostreid herpesvirus OsHV-1. Biology Open 7: bio028134, 10 pp.

Garcia, C., A. Thebault, L. Degremont, I. Arzul, L. Miossec, M. Robert, B. Chollet, C. Francois, J.-P. Joly, S. Ferrand, N. Kerdudou and T. Renault. 2011. Ostreid herpesvirus 1 detection and relationship with Crassostrea gigas spat mortality in France between 1998 and 2006. Veterinary Research 42: 73, 11 pp.

Gittenberger, A., M.A. Voorbergen-Laarman and M.Y. Engelsma. 2016. Ostreid herpesvirus OsHV-1 μVar in Pacific oysters Crassostrea gigas (Thunberg 1793) of the Wadden Sea, a UNESCO world heritage site. Journal of Fish Diseases 39: 105-109.

Gómez-Chiarri, M., X. Guo, A. Tanguy, Y. He and D. Proestou. 2015. The use of -omic tools in the study of disease processes in marine bivalve mollusks. Journal of Invertebrate Pathology 131: 137-154.

Green, T.J. and C. Montagnani. 2013. Poly I:C induces a protective antiviral immune response in the Pacific oyster (Crassostrea gigas) against subsequent challenge with Ostreid herpesvirus (OsHV-1 μvar). Fish & Shellfish Immunology 35: 382-388.

Green, T.J. and P. Speck. 2018. Antiviral defense and innate immune memory in the oyster. Viruses 10: 133, 11 pp.

Green, T.J., C. Montagnani, K. Benkendorff, N. Robinson and P. Speck. 2014a. Ontogeny and water temperature influences the antiviral response of the Pacific oyster, Crassostrea gigas. Fish & Shellfish Immunology 36: 151-157.

Green, T.J., N. Robinson, T. Chataway, K. Benkendorff, W. O'connor and P. Speck. 2014b. Evidence that the major hemolymph protein of the Pacific oyster, Crassostrea gigas, has antiviral activity against herpesviruses. Antiviral Research 110: 168-174.

Green, T.J., D. Raftos, P. Speck and C. Montagnani. 2015a. Antiviral immunity in marine molluscs. Journal of General Virology 96: 2471-2482.

Green, T.J., J.-L. Rolland, A. Vergnes, D. Raftos and C. Montagnani. 2015b. OsHV-1 countermeasures to the Pacific oyster's anti-viral response. Fish & Shellfish Immunology 47: 435-443.

Green, T.J., P. Speck, L. Geng, D. Raftos, M.R. Beard and K.J. Helbig. 2015c. Oyster viperin retains direct antiviral activity and its transcription occurs via a signalling pathway involving a heat-stable haemolymph protein. Journal of General Virology 96: 3587-3597.

Green, T.J., A. Vergnes, C. Montagnani and J. de Lorgeril. 2016a. Distinct immune responses of juvenile and adult oysters (Crassostrea gigas) to viral and bacterial infections. Veterinary Research 47: 72, 11 pp.

Green, T.J., K. Helbig, P. Speck and D.A. Raftos. 2016. Primed for success: Oyster parents treated with poly(I:C) produce offspring with enhanced protection against Ostreid herpesvirus type I infection. Molecular Immunology 78: 113-120.

Grijalva-Chon, J.M., R. Castro-Longoria, J. Ramos-Paredes, T.L. Enríquez-Espinoza and F. Mendoza-Cano. 2013. Detection of a new OsHV-1 DNA strain in the healthy Pacific oyster, Crassostrea gigas Thunberg, from the Gulf of California. Journal of Fish Diseases 36: 965-968.

Guo, X. and S.E. Ford. 2016. Infectious diseases of marine molluscs and host responses as revealed by genomic tools. Philosophical Transactions of the Royal Society B: Biological Sciences 371 (1689): 2015.0206.

Gustafson, L., I. Arzul, C. Burge, R. Carnegie, J. Cáceres-Martínez, L. Creekmore, W. Dewey, R. Elston, C.S. Friedman, P. Hick, K. Hudson, C. Lupo, R. Rheault, K. Spiegel and R. Vasquez Yeomans. 2021. Optimizing surveillance for early disease detection: Expert guidance for Ostreid herpesvirus surveillance design and system sensitivity calculation. Preventive Veterinary Medicine 194: 105419, 9 pp.

Gutierrez, A.P., T.P. Bean, C. Hooper, C.A. Stenton, M.B. Sanders, R.K. Paley, P. Rastas, M. Bryrom, O. Matika and R.D. Houston. 2018. A genome-wide association study for host resistance to ostreid herpesvirus in Pacific oysters (Crassostrea gigas). G3: Genes|Genomes|Genetics 8: 1273-1280.

He, Y., A. Jouaux, S.E. Ford, C. Lelong, P. Sourdaine, M. Mathieu and X. Guo. 2015. Transcriptome analysis reveals strong and complex antiviral response in a mollusc. Fish & Shellfish Immunology 46: 131-144.

Hick, P., O. Evans, R. Looi, C. English and R.J. Whittington. 2016. Stability of Ostreid herpesvirus-1 (OsHV-1) and assessment of disinfection of seawater and oyster tissues using a bioassay. Aquaculture 450: 412-421.

Hick, P.M., O. Evans, A. Rubio, N.K. Dhand and R.J. Whittington. 2018. Both age and size influence susceptibility of Pacific oysters (Crassostrea gigas) to disease caused by Ostreid herpesvirus-1 (OsHV-1) in replicated field and laboratory experiments. Aquaculture 489: 110-120.

Hine, P.M. and T. Thorne. 1997. Replication of herpes-like viruses in haemocytes of adult flat oysters Ostrea angasi: an ultrastructural study. Diseases of Aquatic Organisms 29: 189-196.

Hine, P.M., B. Wesney and B.E. Hay. 1992. Herpes virus associated with mortalities among hatchery-reared larval Pacific oysters Crassostrea gigas. Diseases of Aquatic Organisms 12: 135-142.

Hine, P.M., B. Wesney and P. Besant. 1998. Replication of a herpes-like virus in larvae of the flat oyster Tiostrea chilensis at ambient temperatures. Diseases of Aquatic Organisms 32: 161-171.

Hwang, J.Y., J.J. Park, H.J. Yu, Y.B. Hur, I. Arzul, Y. Couraleau and M.A. Park. 2013. Ostreid herpesvirus 1 infection in farmed Pacific oyster larvae Crassostrea gigas (Thunberg) in Korea. Journal of Fish Diseases 36: 969-972.

ICES. 2018. Report of the Working Group on Pathology and Diseases of Marine Organisms (WGPDMO), 13-17 February 2018,  Riga, Latvia. ICES CM 2018/ASG:01. 42 pp. (see page 9).

Jenkins, C., P. Hick, M. Gabor, Z. Spiers, S.A. Fell, X. Gu, A. Read, J. Go, M. Dove, W. O'connor, P.D. Kirkland and J. Frances. 2013. Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 µ-var) in Crassostrea gigas (Pacific oysters) in Australia. Diseases of Aquatic Organisms 105: 109-126.

Jouaux, A., M. Lafont, J.-L. Blin, M. Houssin, M. Mathieu and C. Lelong. 2013. Physiological change under OsHV-1 contamination in Pacific oyster Crassostrea gigas through massive mortality events on fields. BMC Genomics 14: 590, 14 pp.

Keeling, S.E., C.L. Brosnahan, R. Williams, E. Gias, M. Hannah, R. Bueno, W.L. McDonald and C. Johnston. 2014. New Zealand juvenile oyster mortality associated with ostreid herpesvirus 1 - an opportunistic longitudinal study. Diseases of Aquatic Organisms 109: 231-239.

Lafont, M., B. Petton, A. Vergnes, M. Pauletto, A. Segarra, B. Gourbal and C. Montagnani. 2017. Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas. Scientific Reports 7: 13143, 14 pp.

Lafont, M., P. Goncalves, X. Guo, C. Montagnani, D. Raftos and T. Green. 2019. Transgenerational plasticity and antiviral immunity in the Pacific oyster (Crassostrea gigas) against Ostreid herpesvirus 1 (OsHV-1). Developmental & Comparative Immunology 91: 17-25.

Lafont, M., A. Vergnes, J. Vidal-Dupiol, J. de Lorgeril, Y. Gueguen, P. Haffner, B. Petton, C. Chaparro, C. Barrachina, D. Destoumieux-Garzon, G. Mitta, B. Gourbal, C. Montagnani, J.-L. Imler and N. Pujol. 2020. A sustained immune response supports long-term antiviral immune priming in the Pacific oyster, Crassostrea gigas. mBio 11: 2, 17 pp.

Lassudrie, M., P. Soudant, J.-L. Nicolas, C. Fabioux, C. Lambert, P. Miner, J. Le Grand, B. Petton and H. Hégaret. 2015. Interaction between toxic dinoflagellate Alexandrium catenella exposure and disease associated with herpesvirus OsHV-1 μVar in Pacific oyster spat Crassostrea gigas. Harmful Algae 45: 53-61.

Le Deuff, R.-M. and T. Renault. 1999. Purification and partial genome characterization of a herpes-like virus infecting the Japanese oyster, Crassostrea gigas. Journal of General Virology 80: 1317-1322.

Le Deuff, R.-M., J.L. Nicolas, T. Renault and N. Cochennec. 1994. Experimental transmission of a Herpes -like virus to axenic larvae of Pacific oyster, Crassostrea gigas. Bulletin of the European Association of Fish Pathologists 14: 69-72.

Le Deuff, R.-M., T. Renault and N. Cochennec. 1995. Antibodies specific for channel catfish virus cross-react with Pacific oyster, Crassostrea gigas, herpes-like virus. Veterinary Research 26: 526-529.

Le Deuff, R.-M., T. Renault and A. Gérard. 1996. Effects of temperature on herpes-like virus detection among hatchery-reared larval Pacific oyster Crassostrea gigas. Diseases of Aquatic Organisms 24: 149-157.

Lipart, C. and T. Renault. 2002. Herpes-like virus detection in infected Crassostrea gigas spat using DIG-labelled probes. Journal of Virological Methods 101: 1-10.

López-Sanmartín, M., J.R. López-Fernández, M.E. Cunha, R. De la Herrán and J.I. Navas. 2016a. Ostreid herpesvirus in wild oysters from the Huelva coast (SW Spain). Diseases of Aquatic Organisms 120: 231-240.

López Sanmartín, M., D.M. Power, R. de la Herrán, J.I. Navas and F.M. Batista. 2016b. Experimental infection of European flat oyster Ostrea edulis with ostreid herpesvirus 1 microvar (OsHV-1 μvar): Mortality, viral load and detection of viral transcripts by in situ hybridization. Virus Research 217: 55-62.

López Sanmartín, M., D.M. Power, R. de la Herrán, J.I. Navas and F.M. Batista. 2016c. Evidence of vertical transmission of ostreid herpesvirus 1 in the Portuguese oyster Crassostrea angulata. Journal of Invertebrate Pathology 140: 39-41.

Lynch, S.A., J. Carlsson, A.O. Reilly, E. Cotter and S.C. Culloty. 2012. A previously undescribed ostreid herpes virus 1 (OsHV-1) genotype detected in the Pacific oyster, Crassostrea gigas, in Ireland. Parasitology 139: 1526-1532.

Lynch, S.A., E. Dillane, J. Carlsson and S.C. Culloty. 2013. Development and assessment of a sensitive and cost-effective polymerase chain reaction to detect ostreid herpesvirus 1 and variants. Journal of Shellfish Research 32: 657-664.

Martenot, C. 2013. Les variants du virus herpétique ostreid herpesvirus-1 (OsHV-1) chez l'huître creuse Crassostrea gigas (Variants of herpetic virus ostreid herpesvirus-1 (OsHV-1) in young Pacific oyster Crassostrea gigas). Virologie 17: 81-87.

Martenot, C., E. Oden, E. Travaillé, J.P. Malas and M. Houssin. 2010. Comparison of two real-time PCR methods for detection of ostreid herpesvirus 1 in the Pacific oyster Crassostrea gigas. Journal of Virological Methods 170: 86-89.

Martenot, C., E. Oden, E. Travaillé, J.-P. Malas and M. Houssin. 2011. Detection of different variants of Ostreid Herpesvirus 1 in the Pacific oyster, Crassostrea gigas between 2008 and 2010. Virus Research 160: 25-31.

Martenot, C., S. Fourour, E. Oden, A. Jouaux, E. Travaillé, J.P. Malas and M. Houssin. 2012. Detection of the OsHV-1 μVar in the Pacific oyster Crassostrea gigas before 2008 in France and description of two new microvariants of the Ostreid Herpesvirus 1 (OsHV-1). Aquaculture 338–341: 293-296.

Martenot, C., E. Travaillé, O. Lethuillier, C. Lelong and M. Houssin. 2013. Genome exploration of six variants of the Ostreid Herpesvirus 1 and characterization of large deletion in OsHV-1μVar specimens. Virus Research 178: 462-470.

Martenot, C., O. Lethuillier, S. Fourour, E. Oden, S. Trancart, E. Travaillé and M. Houssin. 2015a. Detection of undescribed ostreid herpesvirus 1 (OsHV-1) specimens from Pacific oyster, Crassostrea gigas. Journal of Invertebrate Pathology 132: 182-189.

Martenot, C., L. Denechère, P. Hubert, L. Metayer, E. Oden, S. Trancart, E. Travaillé and M. Houssin. 2015b. Virulence of Ostreid herpesvirus 1 μVar in sea water at 16°C and 25°C. Aquaculture 439: 1-6.

Martenot, C., N. Faury, B. Morga, L. Degremont, J.-B. Lamy, M. Houssin and T. Renault. 2019. Exploring first interactions between Ostreid Herpesvirus 1 (OsHV-1) and its host, Crassostrea gigas: effects of specific antiviral antibodies and dextran sulfate. Frontiers in Microbiology 10: 1128, 13 pp.

McGladdery, S.E. 1999. Shellfish diseases (viral, bacterial and fungal). In: Woo, P.T.K., D.W. Bruno (eds.) Fish Diseases and Disorders, Volume 3: Viral, Bacterial and Fungal Infections, Vol. 3. CABI Publishing, Wallingford, UK. pp. 723-842.

Mello, D.F., N.M. Danielli, F. Curbani, V.A. Pontinha, S. Suhnel, M.A.M. Castro, S.C. Medeiros, N.C. Wendt, R. Trevisan, A.R.M. Magalhães and A L. Dafre. 2018. First evidence of viral and bacterial oyster pathogens in the Brazilian coast. Journal of Fish Diseases 41: 559-563.

Meyers, T.R. 1981. Endemic diseases of cultured shellfish of Long Island, New York: adult and juvenile American oysters (Crassostrea virginica) and hard clams (Mercenaria mercenaria). Aquaculture 22: 305-330.

Meyers, T.R., T. Burton, W. Evans and N. Starkey. 2009. Detection of viruses and virus-like particles in four species of wild and farmed bivalve molluscs in Alaska, USA, from 1987 to 2009. Diseases of Aquatic Organisms 88: 1-12.

Mineur, F., J. Provan and G. Arnott. 2015. Phylogeographical analyses of shellfish viruses: inferring a geographical origin for ostreid herpesviruses OsHV-1 (Malacoherpesviridae). Marine Biology 162: 181-192.

Miossec, L., G. Allain, I. Arzul, C. Francois, C. Garcia and A. Cameron. 2009. First results of an epidemiological study on oyster (Crassostrea gigas) mortality events in France during summer 2008. Presentation In: 12th ISVEE - International Symposium on Veterinary Epidemiology and Economics (Durban, South Africa), p. 23.

Moreau, P., N. Faury, T. Burgeot and T. Renault. 2015a. Pesticides and ostreid herpesvirus 1 infection in the Pacific oyster, Crassostrea gigas. PLoS ONE 10(6): e0130628, 12 pp.

Moreau, P., K. Moreau, A. Segarra, D. Tourbiez, M.-A. Travers, D.C. Rubinsztein and T. Renault. 2015b. Autophagy plays an important role in protecting Pacific oysters from OsHV-1 and Vibrio aestuarianus infections. Autophagy 11: 516-526.

Morga, B., N. Faury, S. Guesdon, B. Chollet and T. Renault. 2017. Haemocytes from Crassostrea gigas and OsHV-1: A promising in vitro system to study host/virus interactions. Journal of Invertebrate Pathology 150: 45-53.

Morrissey, T., S. McCleary, E. Collins, K. Henshilwood and D. Cheslett. 2015. An investigation of ostreid herpes virus microvariants found in Crassostrea gigas oyster producing bays in Ireland. Aquaculture 442: 86-92.

Mortensen, S., Å. Strand, T. Bodvin, A. Alfjorden, C.K. Skår, A. Jelmert, A. Aspán, L. Sælemyr, L.J. Naustvoll and J. Albretsen. 2016. Summer mortalities and detection of ostreid herpesvirus microvariant in Pacific oyster Crassostrea gigas in Sweden and Norway. Diseases of Aquatic Organisms 117: 171-176.

Moss, J.A., E.M. Burreson, J.F. Cordes, C.F. Dungan, G.D. Brown, A. Wang, X. Wu and K.S. Reece. 2007. Pathogens in Crassostrea ariakensis and other Asian oyster species: implications for non-native oyster introduction to Chesapeake Bay. Diseases of Aquatic Organisms 77: 207-223.

Murray, A.G., M. Marcos-Lopez, B. Collet and L.A. Munro. 2012. A review of the risk posed to Scottish mollusc aquaculture from Bonamia, Marteilia and oyster herpesvirus. Aquaculture 370-371: 7-13.

Nagai, T. and M. Nakamori. 2018. Experimental infection of Ostreid Herpesvirus 1 (OsHV-1) JPType1, a Japanese variant, in Pacific Oyster Crassostrea gigas larvae and spats. Fish Pathology 53: 71-77.

Nicolas, J.L., M. Comps and N. Cochennec. 1992. Herpes-like virus infecting Pacific oyster larvae, Crassostrea gigas. Bulletin of the European Association of Fish Pathologists 12: 11-13.

Normand, J., J.-L. Blin and A. Jouaux. 2014. Rearing practices identified as risk factors for ostreid herpesvirus 1 (OsHV-1) infection in Pacific oyster Crassostrea gigas spat. Diseases of Aquatic Organisms 110: 201-211.

Novoa, B., A. Romero, Á.L. Álvarez, R. Moreira, P. Pereiro, M.M. Costa, S. Dios, A. Estepa, F. Parra and A. Figueras. 2016. Antiviral activity of myticin C peptide from mussel: an ancient defense against herpesviruses. Journal of Virology 90: 7692-7702.

Oden, E., C. Martenot, M. Berthaux, E. Travaillé, J.P. Malas and M. Houssin. 2011. Quantification of ostreid herpesvirus 1 (OsHV-1) in Crassostrea gigas by real-time PCR: Determination of a viral load threshold to prevent summer mortalities. Aquaculture 317: 27-31.

Oliver, R., M. Fuhrmann and P. Hick. 2019. Effect of air exposure, handling stress and imidacloprid on the susceptibility of Crassostrea gigas to Ostreid herpesvirus 1 (OsHV-1). Aquaculture Environment Interactions 11: 685-699.

Pande, A., H. Acosta, N.A. Brangenberg and S.E. Keeling. 2015. Design of a detection survey for Ostreid herpesvirus-1 using hydrodynamic dispersion models to determine epidemiological units. Preventive Veterinary Medicine 119: 80-84.

Paul-Pont, I., N.K. Dhand and R.J. Whittington. 2013a. Influence of husbandry practices on OsHV-1 associated mortality of Pacific oysters Crassostrea gigas. Aquaculture 412–413: 202-214.

Paul-Pont, I., N.K. Dhand and R.J. Whittington. 2013b. Spatial distribution of mortality in Pacific oysters Crassostrea gigas: reflection on mechanisms of OsHV-1 transmission. Diseases of Aquatic Organisms 105: 127-138.

Paul-Pont, I., O. Evans, N.K. Dhand, A. Rubio, P. Coad and R.J. Whittington. 2014. Descriptive epidemiology of mass mortality due to Ostreid herpesvirus-1 (OsHV-1) in commercially farmed Pacific oysters (Crassostrea gigas) in the Hawkesbury River estuary, Australia. Aquaculture 422–423: 146-159.

Peeler, E.J., R. Allan Reese, D.L. Cheslett, F. Geoghegan, A. Power and M.A. Thrush. 2012. Investigation of mortality in Pacific oysters associated with Ostreid herpesvirus-1μVar in the Republic of Ireland in 2009. Preventive Veterinary Medicine 105: 136-143.

Pépin, J.-F. 2013. Short technical report for OsHV-1 detection and quantification by Real Time Polynerase Chain Reaction using OsHV-1 DNA polymerase sequence. ARCHIMER Ifremer's institutional repository, IFREMER, La Tremplade, France, 11 pp.

Pepin, J.F., A. Riou and T. Renault. 2008. Rapid and sensitive detection of ostreid herpesvirus 1 in oyster samples by real-time PCR. Journal of Virological Methods 149: 269-276.

Pernet, F., J. Barret, P. Le Gall, C. Corporeau, L. Dégremont, F. Lagarde, J.-F. Pépin and N. Keck. 2012. Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France. Aquaculture Environment Interactions 2: 215-237.

Pernet, F., F. Lagarde, N. Jeannée, G. Daigle, J. Barret, P. Le Gall, C. Quere and E. Roque d'orbcastel. 2014. Spatial and temporal dynamics of mass mortalities in oysters is influenced by energetic reserves and food quality. PLoS ONE 9(2): e88469, 9 pp.

Pernet, F., D. Tamayo and B. Petton. 2015. Influence of low temperatures on the survival of the Pacific oyster (Crassostrea gigas) infected with ostreid herpes virus type 1. Aquaculture 445: 57-62.

Pernet, F., C. Lupo, C. Bacher and R.J. Whittington. 2016. Infectious diseases in oyster aquaculture require a new integrated approach. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150213.

Petton, B., F. Pernet, R. Robert and P. Boudry. 2013. Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquaculture Environment Interactions 3: 257-273.

Petton, B., M. Bruto, A. James, Y. Labreuche, M. Alunno Bruscia and F. Le Roux. 2015a. Crassostrea gigas mortality in France: the usual suspect, a herpes virus, may not be the killer in this polymicrobial opportunistic disease. Frontiers in Microbiology 6: 686, 10 pp.

Petton, B., P. Boudry, M. Alunno-Bruscia and F. Pernet. 2015. Factors influencing disease-induced mortality of Pacific oysters Crassostrea gigas. Aquaculture Environment Interactions 6: 205-222.

Ren, W., T. Renault, Y. Cai and C. Wang. 2010. Development of a loop-mediated isothermal amplification assay for rapid and sensitive detection of ostreid herpesvirus 1 DNA. Journal of Virological Methods 170: 30-36.

Renault, T. 2006. Les virus infectant les bivalves marins. Annales de l'Institut Pasteur. Virologie,10: 35-41.

Renault, T. 2008a. Genomics and mollusc pathogens: trends and perspective. Journal of Veterinary Clinical Science 1: 4-14.

Renault, T. 2008b. Shellfish viruses. In: Mahy, B.W.J., M.H.V.V. Regenmortel (eds.) Encyclopedia of Virology (Third Edition). Academic Press, Oxford, pp. 560-567.

Renault, T. 2011. Les virus infectant les mollusques marins: un exemple d'actualité, les herpèsvirus. (Viruses infecting marine molluscs: increased mortality outbreaks and herpes viruses.) Bulletin de l'Académie Vétérinaire de France 164: 359-364.

Renault, T. 2016. Chapter 37 - Malacoherpesviruses of Mollusks. In: Kibenge, F.S.B., M.G. Godoy (eds.) Aquaculture Virology. Academic Press, San Diego, pp. 513-524.

Renault, T. and C. Lipart. 1998. Diagnosis of herpes-like virus infections in oysters using molecular techniques. European Aquaculture Society, Special Publication 26: 235-236.

Renault, T. and I. Arzul. 2001. Herpes-like virus infections in hatchery-reared bivalve larvae in Europe: specific viral DNA detection by PCR. Journal of Fish Diseases 24: 161-167.

Renault, T. and B. Novoa. 2004. Viruses infecting bivalve molluscs. Aquatic Living Resources 17: 397-409.

Renault, T., N. Cochennec, R.-M. Le Deuff and B. Chollet. 1994a. Herpes -like virus infecting Japanese oyster (Crassostrea gigas) spat. Bulletin of the European Association of Fish Pathologists 14: 64-66.

Renault, T., R.-M. Le Deuff, N. Cochennec and P. Maffart. 1994b. Herpesviruses associated with mortalities among Pacific oyster, Crassostrea gigas, in France - comparative study. Revue de Médicine Vétérinaire 145: 735-742.

Renault, T., R.-M. Le Deuff, N. Cochennec, B. Chollet and P. Maffart. 1995. Herpes -like viruses associated with high mortality levels in larvae and spat of Pacific oysters, Crassostrea gigas: a comparative study, the thermal effects on virus detection in hatchery-reared larvae. Veterinary Research 26: 539-543.

Renault, T., R.-M. Le Deuff, B. Chollet, N. Cochennec and A. Gérard. 2000a. Concomitant herpes-like virus interactions in hatchery-reared larvae and nursery-cultured spat Crassostrea gigas and Ostrea edulis. Diseases of Aquatic Organisms 42: 173-183.

Renault, T., R.-M. Le Deuff, C. Lipart and C. Delsert. 2000b. Development of a PCR procedure for the detection of a herpes-like virus infecting oysters in France. Journal of Virological Methods 88: 41-50.

Renault, T., C. Lipart and I. Arzul. 2001. A herpes-like virus infecting Crassostrea gigas and Ruditapes philippinarum larvae in France. Journal of Fish Diseases 24: 369-376.

Renault, T., I. Arzul and C. Lipart. 2004. Development and use of an internal standard for oyster herpesvirus 1 detection by PCR. Journal of Virological Methods 121: 17-23.

Renault, T., N. Faury, V. Barbosa Solomieu and K. Moreau. 2011. Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Developmental & Comparative Immunology 35: 725-735.

Renault, T., P. Moreau, N. Faury, J.-F. Pepin, A. Segarra and S. Webb. 2012. Analysis of clinical ostreid herpesvirus 1 (Malacoherpesviridae) specimens by sequencing amplified fragments from three virus genome areas. Journal of Virology 86: 5942-5947.

Renault, T., A.L. Bouquet, J.-T. Maurice, C. Lupo and P. Blachier. 2014a. Ostreid Herpesvirus 1 infection among Pacific oyster (Crassostrea gigas) spat: relevance of water temperature to virus replication and circulation prior to the onset of mortality. Applied and Environmental Microbiology 80: 5419-5426.

Renault, T., G. Tchaleu, N. Faury, P. Moreau, A. Segarra, V. Barbosa-Solomieu and S. Lapegue. 2014b. Genotyping of a microsatellite locus to differentiate clinical Ostreid herpesvirus 1 specimens. Veterinary Research 45: 3, 8 pp.

Robinson, A.N. and T.J. Green. 2020. Fitness costs associated with maternal immune priming in the oyster. Fish & Shellfish Immunology 103: 32-36.

Roque, A., N. Carrasco, K.B. Andree, B. Lacuesta, L. Elandaloussi, I. Gairin, C.J. Rodgers and M.D. Furones. 2012. First report of OsHV-1 microvar in Pacific oyster (Crassostrea gigas) cultured in Spain. Aquaculture 324–325: 303-306.

Rosani, U. and P. Venier. 2017. Oyster RNA-seq data support the development of Malacoherpesviridae genomics. Frontiers in Microbiology 8: 1515, 15 pp.Rosani, U., L. Varotto, S. Domeneghetti, G. Arcangeli, A. Pallavicini and P. Venier. 2015. Dual analysis of host and pathogen transcriptomes in ostreid herpesvirus 1-positive Crassostrea gigas. Environmental Microbiology 17: 4200-4212.

Saulnier, D., J.-F. Pepin, S. Guesdon, L. Degremont, N. Faury, P. Haffner, T. Renault, M.-A. Travers, D. Tourbiez, P. Geairon, O. Le Moine, J.-L. Seugnet and P. Soletchnik. 2011. Mortalités massives de l'huître creuse - Rapport final du programme de recherche sur l'étude de la cinétique de détection d'agents infectieux associés à des épisodes de mortalités de naissains d'huîtres creuses Crassostrea gigas sur un site ostréicole de Marennes-Oléron (CIDAGINF 2009-2010). Contrat de projets Etat-Région Poitou-Charentes 2007-2013. Ifremer, La Tremblade. (in French only)

Sauvage, C., J.-F. Pepin, S. Lapegue, P. Boudry and T. Renault. 2009. Ostreid herpes virus 1 infection in families of the Pacific oyster, Crassostrea gigas, during a summer mortality outbreak: Differences in viral DNA detection and quantification using real-time PCR. Virus Research 142: 181-187.

Sauvage, C., P. Boudry, D.J. De Koning, C.S. Haley, S. Heurtebise and S. Lapègue. 2010. QTL for resistance to summer mortality and OsHV-1 load in the Pacific oyster (Crassostrea gigas). Animal Genetics 41: 390-399.

Schikorski, D., T. Renault, D. Saulnier, N. Faury, P. Moreau and J.-F. Pepin. 2011a. Experimental infection of Pacific oyster Crassostrea gigas spat by ostreid herpesvirus 1: demonstration of oyster spat susceptibility. Veterinary Research 42: 27, 13 pp.

Schikorski, D., N. Faury, J.-F. Pepin, D. Saulnier, D. Tourbiez and T. Renault. 2011b. Experimental ostreid herpesvirus 1 infection of the Pacific oyster Crassostrea gigas: Kinetics of virus DNA detection by q-PCR in seawater and in oyster samples. Virus Research 155: 28-34.

Segarra, A., J.F. Pépin, I. Arzul, B. Morga, N. Faury and T. Renault. 2010. Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Research 153: 92-99.

Segarra, A., L. Baillon, D. Tourbiez, A. Benabdelmouna, N. Faury, N. Bourgougnon and T. Renault. 2014a. Ostreid herpesvirus type 1 replication and host response in adult Pacific oysters, Crassostrea gigas. Veterinary Research 45: 103, 10 pp.

Segarra, A., N. Faury, J.-F. Pépin and T. Renault. 2014b. Transcriptomic study of 39 ostreid herpesvirus 1 genes during an experimental infection. Journal of Invertebrate Pathology 119: 5-11.

Segarra, A., F. Mauduit, N. Faury, S. Trancart, L. Degremont, D. Tourbiez, P. Haffner, V. Barbosa-Solomieu, J.-F. Pepin, M.-A. Travers and T. Renault. 2014c. Dual transcriptomics of virus-host interactions: comparing two Pacific oyster families presenting contrasted susceptibility to ostreid herpesvirus 1. BMC Genomics 15: 580, 13 pp.

Segarra, A., L. Baillon, N. Faury, D. Tourbiez and T. Renault. 2016. Detection and distribution of ostreid herpesvirus 1 in experimentally infected Pacific oyster spat. Journal of Invertebrate Pathology 133: 59-65.

Shimahara, Y., J. Kurita, I. Kiryu, T. Nishioka, K. Yuasa, M. Kawana, T. Kamaishi and N. Oseko. 2012. Surveillance of Type 1 Ostreid Herpesvirus (OsHV-1) variants in Japan. Fish Pathology 47: 129-136.

Tamayo, D., C. Corporeau, B. Petton, C. Quere and F. Pernet. 2014. Physiological changes in Pacific oyster Crassostrea gigas exposed to the herpesvirus OsHV-1 μVar. Aquaculture 432: 304-310.

Tan, T.L.S., I. Paul-Pont, O.M. Evans, D. Watterson, P. Young, R. Whittington, A. Fougerouse, H. Bichet, A.C. Barnes and C. Dang. 2015. Resistance of Black-lip learl oyster, Pinctada margaritifera, to infection by Ostreid herpes virus 1μvar under experimental challenge may be mediated by humoral antiviral activity. Fish & Shellfish Immunology 44: 232-240.

Vásquez-Yeomans, R., J. Cáceres Martínez and A. Figueras Huerta. 2004. Herpes-like virus associated with eroded gills of the Pacific oyster Crassostrea gigas in Mexico. Journal of Shellfish Research 23: 417-419.

Vásquez-Yeomans, R., M. García-Ortega and J. Cáceres-Martínez. 2010. Gill erosion and herpesvirus in Crassostrea gigas cultured in Baja California, Mexico. Diseases of Aquatic Organisms 89: 137-144.

Vigneron, V., G. Solliec, H. Montanié and T. Renault. 2004. Detection of Ostreid Herpesvirus 1 (OsHV-1) DNA in seawater by PCR: Influence of water parameters in bioassays. Diseases of Aquatic Organisms 62: 35-44.

Webb, S.C., A. Fidler and T. Renault. 2007. Primers for PCR-based detection of ostreid herpes virus-1 (OsHV-1): Application in a survey of New Zealand molluscs. Aquaculture 272: 126-139.

Whittington, R.J., P.M. Hick, O. Evans, A. Rubio, B. Alford, N. Dhand and I. Paul-Pont. 2015a. Protection of Pacific oyster (Crassostrea gigas) spat from mortality due to ostreid herpesvirus 1 (OsHV-1 μVar) using simple treatments of incoming seawater in land-based upwellers. Aquaculture 437: 10-20.

Whittington, R.J., N.K. Dhand, O. Evans and I. Paul-Pont. 2015b. Further observations on the influence of husbandry practices on OsHV-1 μVar mortality in Pacific oysters Crassostrea gigas: Age, cultivation structures and growing height. Aquaculture 438: 82-97.

Whittington, R.J., I. Paul-Pont, O. Evans, P. Hick and N.K. Dhand. 2018. Counting the dead to determine the source and transmission of the marine herpesvirus OsHV-1 in Crassostrea gigas. Veterinary Research 49: 34, 21 pp.

Citation information

Bower, S.M. (2021): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Herpes-Type Virus Disease of Oysters.

Date last revised: November 2021
Comments to Susan Bower

Date modified: