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Virus Infections of Scallops

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Category

Category 1 (Not Reported in Canada)

Common, generally accepted names of the organism or disease agent

Virus-like particles. Acute viral necrosis virus (AVNV) or Scallop acute viral necrotic disease (AVND or SAVND)

Scientific name or taxonomic affiliation

Viruses have been reported from various species of scallops. In some cases, the etiological agent of the disease has not be identified. Following is a list of these reports, including more recent information, clustered according to similarity of disease etiology. Available information pertaining to each cluster of reports has the same letter code in subsequent subject headings presented below.

  1. Baculovirus-like particles in 1 epithelial cell of the digestive gland of a clinically healthy scallop (Chang et al. 2002).
  2. Cowdry Type A intranuclear inclusions in the mantle epithelial cells of Crassadoma gigantia contained virus-like particles resembling herpesvirus nucleocapsids (Meyers et al. 2009, Meyer and Burton 2009).
  3. Herpesvirus isolated from Pecten maximus larvae in France. Subsequent PCR and DNA sequencing showed that the virus was a variant of Ostreid herpesvirus type 1 (OsHV-1) that was already described in oysters (Arzul et al. 2001).
  4. The herpesvirus was initially called acute viral necrosis virus (AVNV) and the disease it caused named Acute Virus Necrobiotic Disease (AVND) (Song et al. 2001). The AVNV genome size and its organisation appeared similar to that of Ostreid Herpesvirus type 1 (OsHV-1). Based on its genome sequence and genome organisation (100% identities covering 97% of the complete genome with OsHV-1), Renault et al. (2012) and Ren et al. (2013) considered AVNV to be a variant of OsHV-1 and Bai et al. (2015), Guo and Ford (2016) and Arzul et al. (2017) identified AVNV as OsHV-1.
  5. Virus-like particles associated with cytological changes in digestive and secretory (= basophil) cells in scallops and morphology reminiscent of enteroviruses (Picornaviridae) and caliciviruses (Hine and Wesney 1997). Similar viral infections have been reported from mussels and clams.

Geographic distribution

  1. Abashiri waters of Hokkaido, Japan (Chang et al. 2002).
  2. Two locations (Stedman Cove on Horseshoe Island and Tenass Passage) on the southeastern coast of Alaska, USA (Meyers et al. 2009).
  3. Commercial hatchery in Brittany, France (Arzul et al. 2001).
  4. Northern China, Shandong Province, including Jiaozhou Bay (Wang et al. 2002a, b, c) and Taiping Bay (He et al. 2003) in Qingdao, islands of Changdao county, Yantai and Rongcheng (Bai et al. 2015).
  5. New Zealand (Hine and Wesney 1997)

Host species

  1. Mizuhopecten (=Patinopecten) yessoensis (Chang et al. 2002).
  2. Crassadoma gigantea (Meyers et al. 2009, Meyers and Burton 2009).
  3. Pecten maximus (Arzul et al. 2001, 2017).
  4. Chlamys farreri (Wang et al. 2002a, c; He et al. 2003) and in Mizuhopecten (=Patinopecten) yessoensis from 3 of the islands in Changdao county of Shandong Province (Bai et al. 2015).
  5. Pecten novaezelandiae (Hine and Wesney 1997).

Impact on the host

  1. Virus-like particles were observed in one epithelial cell of the digestive gland of a clinically healthy M. yessoensis during a study on the relationship of histological structures in digestive diverticula to nutrient accumulation (Chang et al. 2002).
  2. Not known. Cowdry Type A intranuclear inclusion bodies were detected in the mantle epithelium of apparently healthy sub-adult (9 of 37 farmed specimens) and adult (1 of 32 wild caught specimens) C. gigantea during a survey for indigenous pathogens by the US Alaska Department of Fish and Game from 1987 to 2009 (Meyers et al. 2009).
  3. A herpesvirus identified as a variant of OsHV-1 was associated with sporadic high mortalities among cultured larval P. maximus in France (Arzul et al. 2001). In the laboratory, mortality reached 100% in 5 days after exposure to extracts from moribund P. maximus larvae whereas, unexposed larvae had a 6% mortality in that time (Arzul et al. 2001). Also, the OsHV-1 extracted from P. maximus was successfully transmitted to oyster (Crassostrea gigas) larvae (Arzul et al. 2001). The detection of OsHV-1 DNA in asymptomatic adult scallops by in situ hybridisation suggests that this herpesvirus may have been transmitted from adults to larvae (Arzul et al. 2001).
  4. In China, AVND (or SAVND) is one of the main causes for large scale mortalities of C. farreir (Tang et al. 2010). During the 1990s following the great expansion and intensification of C. farreir farming, AVND was encountered and became epizootic by 1997. In 1998, the farms in Shandong province, lost 0.18 billion USD directly caused by the massive mortality of cultured scallop (Wang et al. 2002a). For many years, the cause of the scallop mortality in China was unknown, and suspected causes included stress caused by high temperature, overcrowding, starvation and parasites (Guo and Ford 2016). The severe episode in C. farreir (5.0 ± 0.9 cm in shell height) farmed in Jiaozhou Bay in July 6 to August 3, 2000 resulted in 90.0 % accumulated mortality was attributed mainly to a virus (Wang et al. 2002b). The virus initially called AVNV (Song et al. 2001) was later identified as a variant of OsHV-1 (Renault et al. 2012, Ren et al. 2013, Bai et al. 2015, Guo and Ford 2016, Arzul et al. 2017). Acute virus necrobiotic disease usually occurs in 2-year-old adult scallops and peaks in July when water temperatures (25–27°C) are usually highest for the year (Xing et al. 2008). The virus was easily transmitted between scallops in the laboratory using a supernatant prepared from heavily infected scallops to apparently uninfected C. farreir (Wang et al. 2002a, Ai et al. 2003, He et al. 2003, Xing et al. 2008). Several studies have focused on the cellular and molecular responses of C. farreir upon infection with AVNV (Xing et al. 2008; Tang et al. 2010; Chen et al. 2011, 2013, 2014, 2015) and were reviewed by Guo and Ford (2016) and Arzul et al. (2017).
  5. Intermittent mortalities of up to 39% per annum among wild stocks of Pecten novaezelandiae. These sporadic population crashes have made the fishery very difficult to manage, and have resulted in requests to re-stock areas with scallops from other regions. Also, attempts at growing scallops under culture conditions have resulted in mass mortalities (Hine and Wesney 1997).

Diagnostic techniques

Gross observations

  1. None. The infected M. yessoensis appeared clinical healthy.
  2. There was no evidence of overt disease in the infected scallops (Meyers et al. 2009).
  3. High mortality rate (up to 100%) among certain batches of P. maximus larvae in a commercial hatchery (Arzul et al. 2001).
  4. Chlamys farreri with SAVND showed distinct gross signs of lesions in the gills, mantle, kidney, intestine and digestive gland (Wang et al. 2002a). Specifically, typical disease signs in the infected C. farreri include mantle shrinking to the umbo or falling out of the shells, mucus accumulation in the mantle cavity and on the viscera surface, and lack of response to external stimuli (Tang et al. 2010).
  5. None reported excepted moribund condition in P. novaezelandiae from wild and cultured populations experiencing mass mortalities and no lesions were apparent macroscopically (Hine and Wesney 1997).

Histology

Histological examination of the animal on its own is not sufficient to identify a virus infection (Arzul et al. 2017).

  1. Not described. The viral particles were encountered by chance during an ultrastructural study of the digestive gland (Chang et al. 2002).
  2. Cowdry Type A intranuclear inclusion bodies observed in the epithelial cells of the mantle of C. gigantea (Meyers et al. 2009, Meyers and Burton 2009).
  3. Not done.
  4. The typical infection by AVNV in C. farreri was characterized as disordered and necrotic architecture, cellular disruption and disintegration often resulted in empty space amongst the multiple lesions. The epidermis of gill, intestine and mantle sloughed off the basal tissues was often observed. Shedding of the epidermal tissues resulted in the numerical reduction of tubules of the kidney and digestive gland. Cellular changes included nuclear hypertrophy, chromatin margination, pyknosis, karyorrhexis and lastly cellular disintegration in the epithelia and connective tissue cells of the mantle, gills and digestive gland (Wang et al. 2002a, Tang et al. 2010). However, in situ immunofluorescent (IFA) detection of the virus in Davidson's fixed tissue sections revealed fluorescent cells in epithelia of different organs, but not in the epithelium of the digestive diverticula. Cellular lesions revealed by IFA included a disorder or excessive sloughing of the positive epithelial cells in the mantle, kidney and stomach (Fu et al. 2005). Other significant microorganisms were not observed in above-mentioned tissues (Wang et al. 2002a).
  5. All moribund P. novaezelandiae had lesions in the epithelial cells of the distal sections of digestive diverticulae. The shape of most diverticulae appeared normal, but much of the diverticular epithelium resembled empty compartments containing yellowish irregular material in tissue sections stained with haematoxylin and eosin. In the most affected scallops the entire tubule was composed of these 'ghosts' cell, or the compartments had broken down exposing the underlying basement membrane. Damage was extensive and severe in many of the moribund scallops examined and larger scallops tended to possess a higher proportion of affected cells (Hine and Wesney 1977).

Immunological assay

  1. No assays using antibodies were reported.
  2. No assays using antibodies were reported.
  3. No assays using antibodies were reported.
  4. Fu et al. (2005) produced monoclonal IgG antibodies (mAbs) to detect the virus associated with the mass mortalities in cultured C. farreri in China. The mAbs were subsequently used to develop enzyme-linked immunosorbent assay (ELISA, which was not used as a diagnostic tool) and immunofluorescence assay (IFA) which was used to determine that the cytopathological changes and focal lesions corresponded to virus-positive cells in the affected epithelia. They also confirmed by immunogold electron microscopy (IEM) that the mAbs recognized epitopes on the envelope spikes of the virions (Fu et al. 2005).
  5. No assays using antibodies were reported.

Electron microscopy

  1. Several layers of roughly parallel, rod-shaped virions in fence-like arrays. Each virion had a nucleocapsid with a unit membrane envelope and was reminiscent of baculoviruses in morphology. The average length and diameter of the virions were 520 and 130 nm, respectively. The average thickness of the envelope was 12 nm and the average distance between the envelope and the nucleocapsid was 10 nm. No occlusion bodies were observed. The only other abnormality in the infected cell was a great number of small (520 to 1050 nm in diameter), double-membrane vacuoles that appeared to be a network of proliferated, tubular smooth endoplasmic reticulum among the virions (Chang et al. 2002).
  2. Arrays of nuclear particles resembling herpesvirus nucleocapsids were circular or polyconical (about 67 to 75 nm in diameter) with occasional empty capsids (Meyers et al. (2009).
  3. In P. maximus larvae, features of OsHV-1 replication were reported from intranuclear and intracytoplasmic locations and were associated with various cellular lesions, including host cell lysis. Replication involved 2 classes of nucleocapsid; one had an electron-dense core and corresponds to DNA-containing capsids, and the other lacked the core. Intranuclear capsids were circular or polygonal in shape and 74-86 nm in diameter. Naked nucleocapsids were observed in the cytoplasm of lysed cells. In addition, enveloped capsids (virions about 110 nm in diameter) were observed in perinuclear spaces, cytoplasmic vesicles, and extracellular locations (Arzul et al. 2001).
  4. In moribund C. farreri, infection appeared as spherical virus-like particles distributed in a scattered arrangement in the cytoplasmic vesicles (without occluding protein) of infected cells of the kidney, mantle, intestine and digestive gland. The virions were approximately 130 to 170 nm in diameter and had a bilaminal envelope, while the nucleocapsids were 90-140 nm in diameter (Wang et al. 2002a, c). In negative stains of viral isolates, spikes were observed on the viral envelope (Wang et al. 2002a, c).
  5. In P. novaezelandiae, the virus-like particles (22 to less than 36 nm in diameter) were observed in an orderly array on the surfaces of the outer nuclear membrane and along the endoplasmic reticulum of digestive gland epithelial cells. In infected cells, the endocytic and smooth membrane vesicles increased and the endoplasmic reticulum proliferated. Proliferating endoplasmic reticulum membranes were arranged in a reticulated configuration, lined with virus-like particles and enclosed a dense matrix. In some areas, the endoplasmic reticulum cisternae dilated to form vacuolar inclusions containing elongated bodies, spherical in section, in a flocculent matrix and were ornated with virus-like particles arrays on the external membrane.

Molecular characteristics

  1. b. and e. Not known.
  2. Samples of moribund P. maximus larvae were analysed using PCR assays developed for the detection of OsHV-1 and resulting products were sequenced and found to be identical to OsHV-1var or 99% to OsHV-1 (Arzul et al. 2001). Also, in situ hybridisation procedures using digoxigenin-labelled probes developed to detect OsHN-1 detected the virus in apparently healthy adult P. maximus (Arzul et al. 2001).
  3. The AVNV genome from infecting cultured C. farreri in China was sequenced (GenBank accession number GQ153938). The genome consist of a linear, double-stranded DNA molecule of 210,993 bp that is 97% identical to that of Ostreid herpesvirus 1 (OsHV-1) , the amino acid sequences of the encoded proteins of these two viruses are 94-100% identical, and the genomic organization of AVNV contains 3 unique regions in comparison to OsHV-1 (Ren et al. 2013). Renault et al. (2012) described primer pairs that were used to amplify OsHV-1 DNA in a sample from China. Bai et al. (2015) described a nested-PCR procedure to assay for OsHV-1 in bivalves in China. In samples from the coast of Shandong Province, they detected OsHV-1 in 17 samples of C. farreri collected between 2001 and 2013 and in 3 samples of M. yessoensis collected in 2012 and 2013. Also, they used molecular analysis to demonstrate that a separate clade was associated with abnormal mortalities in C. farreri (Bai et al. 2015).

Methods of control

Control and management of viral diseases in molluscs mainly involves active surveillance, implementation of effective biosecurity protocols and other innovations such as mollusc breeding programs targeting production of resistant animals (Arzul et al. 2017). The oyster herpesvirus (OsHV-1) induced high mortalities among larval P. maximus in a commercial hatchery highlights the risks of breeding different species in the same hatchery and indicates the importance of exercising strict precautionary measures to prevent the spread of herpesvirus infections between monocultures (Arzul et al. 2001).

Further specific information is available for AVNV. Experimental results suggested a correlation between elevated seawater temperature and the AVNV associated C. farreri mortalities. Specifically, C. farreri challenged with AVNV at 17°C neither developed notable disease nor showed obvious responses that could be associated with the virus infection (Tang et al. 2010). Guo and Ford (2016) argued that OsHV-1 outbreaks in scallops in China may be caused by increasing ocean temperature as well as culture practices (such as overcrowding cages and grow-out areas) that both increase the likelihood of transmission and stress molluscs making them more susceptible to infection and disease.

References

Ai, H.-x., C.-m. Wang, X.-h. Wang, Y.-j. Liu, Y. Li, J.-y. Huang, G.-z. He and W.-b. Song. 2003. Artificial infection of cultured scallop Chlamys farreri by pathogen from acute virus necrobiotic disease. Journal of Fishery Sciences of China 10(5): 386-391. (In Chinese with English abstract).

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

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

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.

Chang, Y.J., M.-D. Huh, M.-J. Oh and Y. Sugawara. 2002. Baculovirus-like particles in epithelial cell of digestive diverticula of the scallop, Patinopecten yessoensis. Journal of Shellfish Research 21: 109-112.

Chen, G., C. Zhang, C. Li, C. Wang, Z. Xu and P. Yan. 2011. Haemocyte protein expression profiling of scallop Chlamys farreri response to acute viral necrosis virus (AVNV) infection. Developmental & Comparative Immunology 35: 1135-1145.

Chen, G., C. Wang, C. Zhang, Y. Wang, Z. Xu and C. Wang. 2013. A preliminary study of differentially expressed genes of the scallop Chlamys farreri against acute viral necrobiotic virus (AVNV). Fish & Shellfish Immunology 34: 1619-1627.

Chen, G., C. Zhang, F. Jiang, Y. Wang, Z. Xu and C. Wang. 2014. Bioinformatics analysis of hemocyte miRNAs of scallop Chlamys farreri against acute viral necrobiotic virus (AVNV). Fish & Shellfish Immunology 37: 75-86.

Chen, G., C. Zhang, Y. Wang, Y. Wang, C. Guo and C. Wang. 2015. Molecular characterization and immune response expression of the QM gene from the scallop Chlamys farreri. Fish & Shellfish Immunology 45: 543-550.

Fu, C., W. Song and Y. Li. 2005. Monoclonal antibodies developed for detection of an epizootic virus associated with mass mortalities of cultured scallop Chlamys farreri. Diseases of Aquatic Organisms 65: 17-22.

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: 20150206.

He, G.-z., L. Yun, W.-b. Song, C.-m. Wang, J.-y. Huang and X.-h. Wang. 2003. The relationship between pathogenic infection status and motality of the scallop Chlamys farreri. Journal of Fisheries of China 27(3): 273-277. (In Chinese with English abstract).

Hine, P.M. and B. Wesney. 1997. Virus-like particles associated with cytopathology in the digestive gland epithelium of scallops Pecten novaezelandiae and toheroa Paphies ventricosum. Diseases of Aquatic Organisms 29: 197-204.

Meyers, T. and T. Burton. 2009. Diseases of wild and cultured shellfish in Alaska . Fish Pathology Laboratories, Alaska Department of Fish and Game, Anchorage, Alaska, USA.

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.

Ren, W., H. Chen, T. Renault, Y.Y. Cai, C. Bai, C. Wang and J. Huang. 2013. Complete genome sequence of acute viral necrosis virus associated with massive mortality outbreaks in the Chinese scallop, Chlamys farreri. Virology Journal 10: 110, 7 pp.

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(10): 5942-5947.

Song, W.-b., C.-m. Wang, X.-h. Wang, Y. Li and J. Li. 2001. New research progress on massive mortality of cultured scallop Chlamys farreri. Marine Sciences 25(12): 23-26. (In Chinese).

Tang, B., B. Liu, X. Wang, X. Yue and J. Xiang. 2010. Physiological and immune responses of zhikong scallop Chlamys farreri to the acute viral necrobiotic virus infection. Fish & Shellfish Immunology 29: 42-48.

Wang Chong-Ming, Wang Xiu-Hua, Song Xiao-Ling, Wang Yin-Geng, Huang Jie and S. Wei-Bo. 2002a. Possible virus-like etiology causing massive death of scallop Chlamys farreri in northern China. In World Aquaculture 2002 (Beijing, China). Book of Abstracts. World Aquaculture Society, p. 777.

Wang, X.-h., C.-m. Wang, Y. Li, X.-h. Wang, G.-l. Zheng, X.-z. Hu, J. Gong and W.b. Song. 2002b. Epidemiological study on massive death of the cultured scallop Chlamys farreri in the Jiaozhou Bay. Journal of Fisheries of China 26(2): 149-156. (In Chinese with English abstract).

Wang, C.-m., X.-h. Wang, X.-l. Song, J. Huang and W.-b. Song. 2002c. Purification and ultrastructure of a spherical virus in cultured scallop Chlamys farreri. Journal of Fisheries of China 26(2): 180-184. (In Chinese with English abstract).

Xing, J., T. Lin and W. Zhan. 2008. Variations of enzyme activities in the haemocytes of scallop Chlamys farreri after infection with the acute virus necrobiotic virus (AVNV). Fish & Shellfish Immunology 25: 847-852.

Citation information

Bower, S.M. ( 2022): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Virus Infections of Scallops.

Date last revised: April 2022
Comments to Susan Bower

Date modified: