Abalone Viral Ganglioneuritis (AVG)

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• Category
• Common, generally accepted names of the organism or disease agent
• Scientific name or taxonomic affiliation
• Geographic distribution
• Host species
• Impact on the host
• Diagnostic techniques
• Methods of control
• References
• Citation information

Category

Category 3 (Host Not in Canada)

Common, generally accepted names of the organism or disease agent

Abalone herpesvirus (AbHV or AbHV-1), Haliotid herpesvirus 1 (HaHV-1 or HaHV), abalone viral ganglioneuritis (AVG).

Scientific name or taxonomic affiliation

Haliotid herpesvirus 1 (HaHV-1) previously called abalone herpesvirus (AbHV), is the aetiological agent of abalone viral ganglioneuritis (AVG), a contagious disease of abalone species in Australia and coastal areas of the western Pacific Ocean (Hooper et al. 2007, Ellard et al. 2009, OIE 2012, Corbeil et al. 2012a, Crane et al. 2016, Corbeil 2020). Savin et al. (2010) indicated that this neurotropic herpesvirus shares ancestry with the oyster herpesvirus (OsHV-1) and a herpesvirus associated with amphioxus genome (Branchiostoma floridae, an invertebrate chordate). Chen et al. (2012) proposed that HaHV-1 and OsHV-1 may represent 2 viral species, the former infecting gastropods and the latter infecting bivalves. Currently, HaHV-1 (= AbHV) is recognized as a second member of the family Malacoherpesviridae as described by Davison et al. (2009) in the order Herpesvirales (Savin et al. 2010, OIE 2012, Arzul et al. 2017, Rosani and Venier 2017, Bai et al. 2019b) and genus Aurivirus (Crane et al. 2016, and see the International Committee on Taxonomy of Viruses web site).

The icosahedral virus described by Chang et al. (2005) as a putative herpesvirus from farmed Haliotis diversicolor supertexta in Taiwan (Chinese Taipei) was likely HaHV-1 (Burge 2010, OIE 2012, Corbeil 2020). However, Chen et al. (2012, 2014) indicated differences in the pathology in comparison to HaHV-1 in Australian abalone. Specifically, clinical signs in Australian abalone include a swollen mouth and prolapsed odontophore (Hooper et al. 2007), while Taiwan diseased abalone exhibited mantle recession and muscle stiffness (Chang et al. 2005), but lacked the oral lesions observed in Australia (Hooper et al. 2007, Chen et al. 2012). It is not known if such differences are associated with differences in host species response to the same pathogen or if different pathogens were involved (Hooper et al. 2007). Nevertheless, Corbeil et al. (2010) indicated that the TaqMan PCR assay developed as a specific and sensitive technique for the detection of HaHV-1 was able to detect DNA from the Taiwanese abalone herpes-like virus, suggesting a relationship between the Taiwanese and Australian viruses. However, genome sequence analyses have indicated that a number of genotypic variants are present in Australia (Cowley et al. 2011) and further genetic analysis by Chen et al. (2012) suggested that a Taiwan virus isolate (Taiwan/2004) was distinguishable from an Australian HaHV-1 isolate (Victoria/AUS/2007). Chen et al. (2016) determined that another genetic variant of HaHV-1 (referred to as AbHV pathotype associated with chronic mortalities) occurred in Taiwan. Bai et al. (2019b) described the molecular identity of a variant named HaHV-1-CN2003 from Haliotis diversicolor supertexta on the south east coast of China.

The relationship between HaHV-1 and the various reports of viral infections of abalone in China is not known, although there is speculation that at least some of them may be related to HaHV-1 (Burge 2010; OIE 2012; Chen et al. 2012, 2014, 2016; Bai et al. 2019a; Gu et al. 2019). Wei et al. (2018) used metagenomics technology on 3 groups of tissue from moribund Haliotis diversicolor collected between 1999 and 2003 from 2 districts on the south coast of China (Dongshan district, Fujian province and Nanao district, Guangdong province) and detected high levels of AbHV in all 3 groups and high levels of Shriveling Syndrome-associated Virus (AbSV) in one group with lower levels in the other two.

Note that the virus associated with AVG is not the same as the viral infections of glioma which causes Amyotrophia of Abalone in Japan. However, the viruses considered in 2 of the reports from Japan (i.e., Otsu and Sasaki 1997 and Nakatsugawa et al. 1999) were included as herpes-like viral pathogens by Chen et al. (2012).

Geographic distribution

South eastern Australia (Victoria (Hooper et al. 2007, Corbeil 2020) and possibly Tasmania (Ellard et al., 2009)), south east coast of China (Wei et al. 2018, Bai et al. 2019a, Gu et al. 2019) and Taiwan (Chang et al. 2005, Chen et al. 2016). In contrast to the situation in Victoria, AVG has not occurred in farmed abalone in Tasmania nor in wild abalone in Tasmanian open waters (Crane et al. 2009a). However, after active surveillance in Tasmania for AVG on abalone farms and in wild abalone populations between June 2006 and July 2008 and subsequent extensive testing of wild abalone stocks in September to December 2009 (1780 abalone) by PCR and histopathology only one sample was PCR positive leading to the suggestion that very low levels of subclinical infections with AVG could be present in Tasmanian wild stocks (Ellard et al. 2009).

Host species

Haliotis laevigata, Haliotis rubra and their hybrids (OIE 2012) and Haliotis conicopora (Corbeil et al. 2016) were susceptible to infection and disease caused by HaHV-1 in Australia as was Haliotis diversicolor from the southern coast of China (Wei et al. 2018). In Taiwan, HaHV-1 caused mortality in Haliotis diversicolor supertexta  but not to cohabitating Haliotis discus which remained normal (Chang et al. 2005). Similar results were obtained during laboratory exposure (by injection, immersion and cohabitation) to HaHV-1 with H. diversicolor supertexta being highly susceptible to infection resulting in acute mortality while Halitois discus hannai was not susceptible to infection (Bai et al. 2019a). During an epidemiological study on HaHV-1 in samples of mainly healthy abalone collected from farms in south China between 2002-2013, Gu et al. (2019) detected the virus in H. diversicolor and H. discus hannai at similar rates of infection. However, HaHV-1 did not cause disease in H. discus hannai but some samples of H. diversicolor collected before 2012, and presumed to comprise diseased animals, had ultra-high HaHV-1 DNA loads and 1 batch of H. diversicolor collected in July 2013 that was experiencing high mortality had a 66.67% detection rate of HaHV-1 (Gu et al. 2019). Experimental investigations indicated that Haliotis iris (the New Zealand paua) was highly resistant to infection by HaHV-1 and fully resistant to AVG (Corbeil et al. 2017, Neave et al. 2019, Corbeil 2020).

Impact on the host

Abalone viral ganglioneuritis (AVG), caused by HaHV-1, is a disease that has been responsible for extensive mortalities in wild and farmed abalone and has caused significant economic losses in Asia and Australia since outbreaks occurred in the early 2000s (Corbeil 2020). In Taiwan in January 2003, the high mortality of farmed H. diversicolor supertexta (in both land-based and ocean-based ponds) was attributed to a herpes-like virus (Chang et al. 2005). Both adult and juvenile abalone suffered from the disease, with cumulative mortalities of 70 to 80% and the death of all of the abalone in a pond could occur within 3 days of the onset of clinical signs in 16-19 ºC water (Chang et al. 2005). Similarly in Victoria, Australia, outbreaks of AVG in both farmed and wild abalone populations were associated with the rapid onset and high mortality rates (up to 90%) in all age classes (Corbeil et al. 2010, Mayfield et al. 2011, Crane et al. 2016, Corbeil 2020). The disease was first detected in farmed abalone in Victoria, Australia in December 2005 and then in wild population in May 2006 (Hooper et al. 2007, Appleford et al. 2008). Mortality levels typically ranged between 30 to 90% varying between and within reefs (Appleford et al. 2008, Conrad and Rondeau 2015). A similar disease pattern occurred with experimental infections (Chang et al. 2005, Crane et al. 2009a, Corbeil et al. 2012a, OIE 2012) and the disease agent was identified as Abalone herpesvirus (AbHV) and formally named Haliotid herpesvirus-1 (HaHV-1) (Crane et al. 2016).

Transmission studies found HaHV-1 was spread via direct contact and by water (horizontal transmission), with infectivity readily reduced by dilution and HaHV-1 was probably moving on agents when it travelled several kilometers in the field (Appleford et al. 2008).

Corbeil et al. (2011, 2012a) determined that abalone, experimentally bathed in seawater into which diseased abalone had shed infectious viral particles, tested positive for the presence of viral DNA by real-time PCR as early as 36 hours after challenge. The ISH assay detected the virus in tissues as early as 48 hours post-exposure and the exposed abalone began displaying gross signs of AVG 60 hours after immersion (Corbeil 2020). Crane et al. (2016) suggested that preclinical (before the onset of clinical signs of disease) excretion of the virus may occur. Also, results of exposure experiments suggested that the surviving wild abalone from within the geographical range for AVG were not resistant to HaHV-1 and were probably not exposed to pathogenic doses of the virus during the initial outbreak that commenced in 2006 and spread along the coast of Victoria, Australia (Crane et al. 2013). Corbeil et al. (2016) determined that 5 known variants of HaHV-1 caused disease and mortality in all abalone stocks tested (H. laevigata, H. rubra and H. conicopora). Corbeil (2020) indicated that since 2011, a regular surveillance program maintained by Australia has not reported a case of AVG but this disease is still worrisome for abalone production. However, Corbeil (2020) indicated that in 2020, Taiwanese farmed abalone still suffered from AVG, putting financial hardship on the industry. In China, following the severe impact of AVG, the Chinese abalone industry has moved away from growing the susceptible species H. diversicolor supertexta and has since reported few cases of AVG (Corbeil 2020).

Dang et al. (2013) characterized the immune parameters of hybrid abalone (Haliotis laevigata X Haliotis rubra) following HaHV-1 challenge. Measurements performed included total hemocyte count (THC), detection of superoxide anion (SO) and antiviral activity against herpes simplex virus 1 (HSV-1). These parameters were examined in apparently healthy (subclinical) and moribund abalone after challenge. The presence of AbHV in the abalone negatively correlated with THC and SO levels. The anti-HSV-1 activity of abalone plasma did not increase above baseline levels in response to experimental infection with HaHV-1 (Arzul et al. 2017). In conclusion, Dang et al. (2013) suggested that abalone mount an initial cellular immune response to HaHV-1 infection, but this response cannot be sustained under high viral loads, leading to mortality. Bai et al. (2019c) used dual transcriptomeic analysis to determine that HaHV-1, at least at the beginning of infection, can replicate with no activation of an immune response from H. diversicolor supertexta and suggested that the virus could evade the abalone immune surveillance at the early stage of infection.

Although genetic traits of virus resistance in gastropods have not been extensively investigated, some family lines of H. laevigata showed a slight increase in resistance to infection by the abalone herpesvirus (Arzul et al. 2017). Neave et al. (2019) used whole transcriptome analysis to investigate the natural resistance of H. iris to AVG and suggested that the results may support the development of molecular therapeutics useful in the control and/or management of viral outbreaks in abalone culture. Aguis et al. (2020) reviewed the immune control of herpesviruses in molluscs including a summary of the literature on the immune responses of abalone infected with HaHV-1 and indicated that many gaps still exist in the understanding of possible immune based strategies for controlling HaHV-1 in abalone.

Diagnostic techniques

The presence of HaHV-1 should be suspected if affected abalone display clinical signs and pathology as described below. In addition to clinical signs and consistent pathology, the presence of HaHV-1 can be confirmed using molecular assays. Specifically, the virus is positively identified in tissue sections by in situ hybridisation and/or by real-time (TaqMan) PCR or conventional PCR followed by sequence analysis of the amplicon to demonstrate virus identity (Crane et al. 2009a, 2016).

Gross observations

In Australia, a variable proportion of affected abalone may demonstrate irregular peripheral concave elevation of the foot, swollen turgid mouth parts which protruded anterior to the pedal muscle (Crane et al. 2009a). In severe cases, the radula protruded from the prolapsed mouth and outlines of the 2 odontophores (cartilagenous plates normally interior to the mouth) were visible. In some affected abalone, the radula was completely everted and hung limply (Hooper et al. 2007, Crane et al. 2016). Gross signs of pustules and blisters observed on the foot of infected animals are also considered as indicative of AVG (Arzul et al. 2017). In the field, active signs of the viral infection include:

• infected animals losing muscle control
• minimal movement of the pedal muscle
• excessive mucus production
• absence of the marked extension of the foot shown in the righting reflex when healthy abalone are turned onto their backs and reduced pedal adhesion to the substrate (Crane et al. 2009a).

In areas with high mortalities, large numbers of intact moribund abalone, shiny empty shells and loose meats rolling around in the wash were typical signs of the disease (Prince 2007). Ellard et al. (2009) noted that H. laevigata and H. rubra from the coast of Tasmania held in tanks of a live-holding facility showed paralysis, stiffness of the muscle and mantle, and excessive mucus production but no elevated mortality. In Taiwan, clinical signs of disease in H. diversicolor supertexta were mantle recession and muscle stiffness associated with high mortalities (Chang et al. 2005).

Histology

The major histopathological lesion is ganglioneuritis (haemocyte proliferation or infiltration confined to neural tissue starting in the gray matter and extending into the white matter and perineural sheath) associated with focal neuron degeneration and possibly associated cell necrosis (Crane et al. 2009a, Corbeil et al. 2012a, Arzul et al. 2016, Bai et al. 2019a, Corbeil 2020). Neural tissue that includes the cerebral, pleuropedal (see photograph in Crane et al. (2016) for the location of the pleuropedal ganglion in abalone) and buccal ganglia is the best tissue to examine for lesions and lesions have not been detected consistently in non-neural tissues (OIE 2012).The ganglia and surrounding neurilemma can be affected as well as the cerebral commissure and peripheral nerves in some cases (Hooper et al. 2007, OIE 2012). Occasionally, neurons had nuclei with emarginated chromatin with morphological features suggestive of intranuclear viral inclusions but no Cowdry type A inclusions were observed (Hooper et al. 2007). In Taiwan, the nerve system of infected abalone was also reported to be the primary target tissue (Chang et al. 2005). However, the AbHV pathotype found in H. diversicolor from Taiwan with chronic infections showed haemocyte infiltration in the lamina propia of the digestive tract with haemocytes of various stages present and loss of seminal tubules in the gonad (Chen et al. 2016). Bai et al. (2019a) also reported heavy haemocyte infiltration in the haemolymph vessels and connective tissue between digestive gland tubules and high magnification revealed nuclei with chromatin marginalization and pykinosis. Caraguel et al. (2019) determined that histopathology had very poor diagnostic sensitivity for HaHV-1 in sub-clinical abalone with limited pathological change. However, they recommended histopathology when clinically investigating outbreaks (mortality events) to find potential new, emerging HaHV-1 genotype(s) that may not be detectable by the more sensitive PCR assays (Caraguel et al. 2019).

Electron microscopy

Infected cells (haemocytes and possibly glial cells) may show damage to the nuclear membrane, swelling of the mitochondria and proliferation of the endoplasmic reticulum. The virus replicates in the nucleus and maturation takes place in the cytoplasm of infected cells. The intranuclear viral capsids (70-100 nm in diameter) occur in the nucleus and enveloped virions (90-165 nm in diameter with a two-layer envelope (8-10 nm)) are assembled in the cytoplasm (Corbeil et al. 2012a, Arzul et al. 2017, Corbeil 2020). Similar herpes-type viruses were reported in H. diversicolor supertexta in Taiwan (Chang et al. 2005, Chen et al. 2012). Bai et al. (2019a) published transmission electron micrographs of herpesviruses identified as HaHV-1 in H. diversicolor supertexta from the south east coast of China. Corbeil et al. (2012a) and Crane et al. (2016) indicated that viral particles often occur in relatively low numbers difficult to detect even in cases of acute disease. Tan et al. (2008) purified the virus from H. laevigata, H. rubra and hybrids by ultracentrifugation on a sucrose gradient prepared in sea-water. Transmission electron microscopy of the negatively stained purification revealed virus particles with an icosahedral capsid surrounded by an envelope with numerous spikes on the external surface. The capsid ranged from 92-109 nm in diameter and the enveloped virus was about 150 nm in diameter (Tan et al. 2008, Crane et al. 2016).

DNA probes

In order to detect HaHV-1 infection in the absence of clinical disease, the genome of HaHV-1 was sequenced and sensitive molecular diagnostic techniques were developed and validated (Crane et al. 2009a, 2016; Chen et al. 2012; Corbeil 2020). Conventional polymerase chain reaction (PCR) was described for the identification of HaHV-1 in clinically affected animals; a real-time (TaqMan) PCR method was developed which can detect HaHV-1 in sub-clinically infected abalone; and an in situ hybridisation (ISH) test has been developed for the localisation of virus associated with histopathology in tissue sections (Crane et al. 2009a, b, 2016; Fegan et al. 2009; Corbeil et al. 2010, 2012a; Mohammad et al. 2011; OIE 2012; Corbeil 2020). These tests were used to estimate the geographical range of HaHV-1 which includes regions of Victoria and Tasmania, even though disease has not been observed in Tasmanian open waters or farms (Crane et al. 2009a). Bai et al. (2019a) also used TaqMan PCR to identify HaHV-1 in the nervous tissue and digestive gland of H. diversicolor supertexta from the south coast of China. However, Cowley et al. (2011) indicated that sequence variation occurred in the genome region targeted by the TaqMan PCR because the test failed to amplify an HaHV-1 strain from Tasmania. Nevertheless, pathology was consistent with AVG, the isolate was induced in experimental bioassays, the virus was associated with tissue lesions by in situ hybridisation, and a herpes-like virus was detected by electron microscopy. Further analysis indicated that at least 2 discrete genotypic variants occurred in Tasmanian abalone and these variants were different from the apparently homogenous isolates from various locations in Victoria collected at different times (Cowley et al. 2011). Although the TaqMan PCR assay described by Corbeil et al. (2010) was able to detect DNA from the Taiwanese abalone herpes-like virus, Chen et al. (2012) developed a classical PCR-based procedure for detecting herpesvirus infection of H. diversicolor supertexta in Taiwan. Gao et al. (2018) developed a real-time quantitative recombinase polymerase amplification (qRPA) with an optimal reaction temperature of 37°C and took 20 min for the detection of AbHV, an approach they found to be faster and more sensitive than qPCR.

Caraguel et al. (2019) tested the accuracy of 3 real-time PCR assays and determined that 2 of them interpreted in parallel performed the best both analytically and diagnostically to demonstrate freedom from HaHV-1 in an established population of abalone and to certify individual abalone free from HaHV-1 for trade or movement purposes. Chen et al. (2014) developed a loop-mediated isothermal amplification (LAMP) procedure which amplified nucleic acids from the herpesvirus of H. diversicolor supertexta with high specificity, sensitivity and rapidity under isothermal conditions. Corbeil (2020) indicated that the LAMP assay was fast, sensitive, specific, low cost and suitable for field application. In Taiwan, Chen et al. (2016) used ISH to reveal that in HaHV-1 acute infections, positive signals were restricted to the neural ganglia, while in AbHV pathotype chronic infections, positive signals were observed only in the haemocytes suggesting that the tropism of HaHV-1 shifted from mainly neurotropic in HaHV-1 acute infections to mainly haemocytotropic in abalone suffering from chronic mortality.

Methods of control

To date, there are no effective treatments for AVG and currently control methods rely on surveillance, biosecurity systems at farms and processing premises, zoning and restrictions on the movement of live abalone, and rapid response and decontamination systems to contain disease occurrences. Farm disease outbreaks are managed through the destruction and safe disposal of affected abalone, disinfection of water and equipment, and following procedures to effectively prevent recurrences (Crane et al. 2016). Infected abalone should not be transported into areas known to be free of the disease. For example, in Western Australia, Jones and Fletcher (2012) recommended strategies to mitigate the risk of introducing AVG to wild abalone stocks via the release of juvenile abalone from hatcheries. The OIE (2012) recommends the implementation of high levels of on-farm and live-holding facility biosecurity and regional movement restrictions. Appleford et al. (2008) indicated that specific biosecurity protocols were developed and implemented with research efforts focusing on biosecurity, stock rebuilding and epidemiology. Conrad and Rondeau (2015) presented a spatial bioeconomic stylized model dealing with the spread of AVG in a patchy environment along the coastline of Victoria, Australia. The following link on Abalone Viral Ganglioneuritis (AVG) provides an overview of this abalone disease.

Assays designed to assess the efficacy of chemical treatments showed that iodophors (e.g., Buffodine at 50 ppm) and a non-ionic surfactant (e.g., the detergent 'Impress' at 1 %) fully inactivated the virus after 10 min. exposure while calcium hypochlorite (20 ppm free chlorine) demonstrated only partial inactivation as assessed via injection into naïve abalone (farmed hybrids of H. rubra x H. laevigata) after HaHV-1 exposure to one of the three compounds (Corbeil et al. 2011, 2012b). However, calcium hypochlorite (at 10 to 15 ppm to give 1.5 to 2.0 ppm residual chlorine) inactivated HaHV-1 (1.67 x 10⁶ viral genome copies (v.g.c.)/mL) when assessed by immersion challenge of naïve abalone (farmed hybrids of H. rubra x H. laevigata) for 15 minutes (Corbeil et al. 2011, 2012b). Thus, the iodophor Buffodine and the non-ionic surfactant 'Impress' are very effective virucidal agents under experimental conditions while calcium hypochlorite is also effective but on lower virus concentrations (Corbeil et al. 2012b, Corbeil 2020).

In abalone farms in Australia, the role of stress factors including high densities, spawning period and water temperature was highly suspected as contributing factors to the high mortality rates (Hooper et al. 2007, Arzul et al. 2017). Corbeil et al. (2012b) indicated that HaHV-1 stability in the water column is modulated by temperature and infectivity/pathogenicity is reduced by 100% within a few days under experimental conditions. Specifically, the virus was held at 4, 15, or 25°C for 1, 5, and 12 days prior to immersion challenge of naïve abalone (farmed hybrids of H. rubra x H. laevigata). Mortality curves indicated that when held for 1 day in sea water at 4°C and 15°C the virus remained infectious and highly pathogenic. In addition, the virus retained partial infectivity after 5 days held at 4°C but only a few non-disease related abalone mortalities were detected under the other experimental conditions (Corbeil et al. 2012b). Corbeil et al. (2016) speculated that the Tasmanian virus variants remain sub-clinical in Tasmanian wild abalone because environmental conditions (for example, water temperature) favour a latent or persistent infection.

Early attempts to improve AVG resistance amongst abalone family lines indicated that the small degree of delay to mortality rather than overall survival did not justify the required lengthy and expensive breeding program (Corbeil 2020). When Corbeil et al. (2017) demonstrated that H. iris was highly resistant to AVG, further studies at the gene transcriptional level showed that the H. iris upregulated broad classes of genes that contained chitin-binding peritrophin-A domains (Neave et al. 2019). Haliotis iris  also mounted an acute inflammatory response, including the upregulation of VAP-1 (an important adhesion molecule for lymphocytes in mammals), and blood coagulation pathways were broadly dysregulated (Neave et al. 2019). Also, identifying the mechanisms of resistance in H. discus hannai (Bai et al. 2019a) and comparing these mechanisms with those of H. iris may provide insights into methods for developing or selecting for resistance in farmed Haliotis spp. currently susceptible to AVG. Corbeil (2020) also discussed the possibility of developing procedures of molecular vaccination or other molecular therapeutics for increasing resistance in vulnerable stocks.

Storage of HaHV-1 in liquid nitrogen maintained viral infectivity and pathogenicity for at least 21 months whereas isolates stored at -80°C lost some viability by 12 months and isolates at -20°C lost significant viability by this time (Williams et al. 2009).

References

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Citation information

Bower, S.M. (2022): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Abalone viral ganglioneuritis (AVG).

Date last revised: January 2022
Comments to Susan Bower