A parvovirus is a small, non-enveloped DNA virus that infects a variety of animals. The viruses have been named according to the isolated hosts rather than their genetic associations (51). Currently, the International Committee on Taxonomy of Viruses stipulates that the waterfowl parvovirus belongs to the
Goose parvovirus is an important virus that can infect goslings and Muscovy ducks. It can cause Derzsy's disease, which has a mortality rate exceeding 50% in epidemic years and is highly contagious (9,14). The most typical clinical feature of the disease is the intestinal plug formed by the coagulation of fibrinous exudate and intestinal mucosal necrotic detachment. Depending on the course of the disease, it is classified into peracute, acute and subacute types (2). At present, the Derzsy’s disease vaccines on the market can prevent Derzsy’s disease. Researchers are developing a convenient, non-toxic and more effective goose parvovirus vaccine (28).
MDPV causes high morbidity and mortality in ducklings under 3 weeks of age (40, 58, 65). The main clinical symptoms of this disease include wheezing, motor dysfunction and diarrhoea (31). In general, the mortality rate of infected Muscovy ducks over 3 weeks of age is much lower than that of younger birds, but survivors usually show symptoms of skeletal muscle degeneration and growth retardation (55). In 2015, an unidentified infectious disease broke out for the first time in a flock of Cherry Valley ducks in eastern China. It was manifested in a short beak and growth retardation has come to be known as beak atrophy and dwarfism syndrome (BADS). This infectious disease can cause 20% to 50% morbidity. Although the mortality rate of short beak and dwarfism syndrome (SBDS), (a synonym of BADS) is very low, the severe weight loss caused by stunting has caused serious economic losses to the Chinese waterfowl industry (21). The pathogen was found to be a variant strain of GPV –NGPV, also referred to in some research as short beak and dwarfism syndrome virus (SBDSV).
The group of waterfowl parvoviruses combines NGPV, GPV and MDPV. They share similarities in morphology, physicochemical properties, culture characteristics and genomic structure, but their pathogenicity and antigenicity are quite different. There is a genetic relationship between GPV, MDPV and NGPV, and the biological characteristics of and detection methods for the three have attracted more researchers’ attention. In this review, the pathogenic characteristics, clinical symptoms, and genetic relationship of the three parvoviruses and necropsy characteristics of infected ducks are expounded, and the findings on the genetic relationship of the three viruses will provide reference material for further research.
Parvoviruses are non-enveloped single-stranded DNA viruses, which include 23 genera and 107 species, usually characterised by a single-stranded DNA genome, and can be further classified into the
In the structural proteins VP1, VP2 and VP3, the peptide chain of VP1 is longer than that of VP2, and in turn its chain is longer than that of VP3 (34). The entire amino acid sequence of VP2 and VP3 is contained in the carboxyl terminal portion of VP1 (43). The VP1, VP2 and VP3 genes are located in the “basket structure”, which means that they have the same gene sequence and the same termination codon in the 3′ end region, but their initiator codons are located at different positions (38, 42, 44). The 58-kDa molecular weight VP3 protein is the main capsid protein of the virus, main protective antigen and contains the main epitope of the virus. This protein can induce the body to produce neutralising antibodies and provide protective cross-immunity to other waterfowl parvoviruses; results of investigations showed that the VP3 protein is the main candidate antigen for vaccine development and serodiagnostic tests (22, 56, 63). Of these three capsid proteins, accounting for about 80% of the total capsid protein amount, VP3 is the largest element and can serve as a scaffold protein (40). The VP2 protein is highly immunogenic, easily inducing antibodies in ducks and geese, and is abundant during viral infection (59, 20).
This protein has different functions throughout the life cycle of the virus and can also take part in shell assembly and DNA packaging(18) (Fig. 1).
The main characteristics of Derzsy’s disease caused by GPV is high mortality, and the main clinical symptoms include somnolence, ataxia, dysphagia, weight loss, bilateral periorbital, eyelid swelling and frequent yellowish-white diarrhoea. Goslings infected with GPV convulse before death, and mortality rates in the first four weeks of life reach 70% to 100% (15, 25, 32, 57).
MDPV only affects ducklings (2–4 weeks old) and the mortality from its associated disease is up to 80% depending on the age of the infected Muscovy duck. The characteristic symptoms of MDPV infection are watery diarrhoea, wheezing and locomotor dysfunction (13, 16, 19, 49).
The SBDS caused by NGPV occurs primarily in ducks which are 10 to 30 days old. Some ducklings were unable to walk at 5 to 6 days of age and some were found to be growing slowly at 9 to 10 days of age. The shortness and poor growth of the ducks were more evident after 3 weeks of age. Ducks infected with NGPV also showed weakness in the feet, suffered fractures of the tibia and exhibited truncation of the beak. The disease does not cause high mortality but in its clinical incidence of up to 60% (12) it is grave in its impact. The final beak size of a duckling suffering from SBDS is about 10–30% of the normal beak size of healthy ducklings. Beak dysplasia causes the infected ducks’ tongues to protrude, and this significantly affects their eating ability. The body weight of infected ducks when brought to market is 20–30% lower than that of healthy ducks, and the most serious infected ducks are 50% lighter. Furthermore, some of the ducks suffer from walking difficulty with a unilateral dysfunction, paralysis and other symptoms (35, 39, 57).
Most of the corpses of geese infected with GPV are visibly thin, the eye sockets are depressed, the mouth has a lot of secretions, the oral mucosa is brown, and the whole body has subcutaneous haemorrhages, there is pleural effusion, fatty degeneration in the liver and gallbladder, kidney swelling, and congestion in the pancreas and spleen. The mucosa in the middle part of the small intestine of a typical goose is necrotic and shows shedding, while the lower part of the small intestine forms a sausage-like embolus, and the intestinal lumen is blocked. Haematoxylin and eosin staining of paraffin-fixed tissue sections showed hepatic congestion and inflammatory cell infiltration, villous necrosis, shedding, duodenal, ileal and jejunal mucosa with the presence of inflammatory cells and cellulose-like exudate, dilation of capillaries in the brain and turbidity of renal tubular epithelial cells (52). Liu
It can be observed in MDPV duck necropsies that most of the cloaca is surrounded by thin faeces, the heart has assumed a round shape and its wall is slack, the liver is swollen and brittle, the spleen is swollen. There are white necrotic spots in the pancreas, intestinal catarrhal inflammation, haemorrhaging, congestion and exfoliated intestinal mucosa in the intestinal contents. Decreased the body skeletal muscle mass and pallor of the leg skeletal muscles were observed in some MDPV duck necropsies (13, 16, 37).
In ducks infected with novel GPV, the lesions are quite different from those in ducks infected with the other two viruses. In addition to the short beak and long tongue, some ducks infected with NGPV have scattered bleeding spots or diffuse bleeding on the surface of the pancreas, as well as swelling in the liver, spleen, kidney, lung, small intestine, and pancreas. Thymic medullary lymphocytes and reticular cells show scattered necrosis, inflammatory cell infiltration, and tissue interstitial bleeding, the renal tubules also have interstitial haemorrhaging, and heavy inflammatory cell infiltration, and tubular epithelial cells present with disintegration and apoptosis. Hepatocytes diffusely infiltrate macrophages in the hepatic lobules and show other histopathological changes, such as hepatocyte swelling and steatosis, as well as various sizes of fat droplets in the cell mass. Moderate tongue lesions are characterised by interstitial inflammation, connective tissue interstitial loosening and oedema (5).
According to the sequence analysis of the waterfowl parvovirus genes, there are two important amino acid changes (Asn-489 and Asn-650) in the VP protein of NGPV compared with GPV, which may be the only reason why the host of GPV changed from the goose to the duck. By immunological epitope prediction, the aa515–aa528 region in NGPV is considered to be the binding site of the VP3 domain, which will trigger the production of neutralising antibodies. The discovery of this immunological epitope makes an important contribution to the development of a vaccine against SBDS (30). After continuous passages in duck embryos, SBDSV M15 was isolated from the allantoic fluid of dead embryos, and its nucleotide and amino acid homology with Hungarian GPV strains and Chinese GPV strains was 96.0–97.1% and 97.4–98.3%, respectively. Seven SBDS duck samples were found to be positive for GPV antigen by a latex agglutination assay, while being negative for MDPV. As a consequence, it was found that SBDSV M15 is a strain of a novel parvovirus associated with GPV that causes SBDS (6). In order to confirm the pathogenicity of SBDSV M15 in other domestic waterfowl species, three day old Muscovy ducks, sheldrake ducklings and goslings without GPV antibodies were infected with a high dose of SBDSV M15. It is seen in Table 1 that Muscovy ducks infected with SBDSV M15 lost 41%, 43%, and 57.5% of body weight at 14, 21, and 28 days post infection (dpi), respectively compared with the control group. The weight of the sheldrake ducklings infected with SBDSV M15 lost 5.9%, 23.6%, 27.9% at these three intervals. The rates of weight loss in gosling infection group were 19.0%, 32.0%, 36% at 14, 21, and 28 dpi, respectively (Table 1). In summary, it was found that SBDSV M15 is pathogenic to Muscovy ducks, sheldrake ducklings and goslings. The infected birds were found to exhibit significant growth retardation, anorexia and diarrhoea; however, no atrophied tendons or protruding tongues were observed in any inoculated birds. These results indicated that the emerging duck-derived goose parvovirus in China has extensive pathogenicity to major domestic waterfowl, and its symptoms are diverse. With deleterious effects such as were noted in the research, SBDS may inflict huge economic losses on the Chinese waterfowl industry (53).
Inhibited the body weights growth trend of three waterfowl species after infection with SBDSV M15
Infected waterfowl | Inhibited the percentage of weight gain compared with the control group |
||
---|---|---|---|
14 dpi | 21 dpi | 28 dpi | |
Muscovy duck | 41.0% | 43.0% | 57.5% |
Sheldrake ducklings | 5.9% | 23.6% | 27.9% |
Goslings | 19.0% | 32.0% | 36.0% |
Detection of GPV and NGPV by recombinase polymerase amplification (RPA) combined with vertical flow visualisation bands is more efficient than the loop-mediated isothermal amplification technique and provides an important diagnostic tool for detecting GPV and NGPV infections because it has high sensitivity and specificity and the RPA reagent is provided as lyophilised granules for easier storage and transport (27). Li
Description of waterfowl parvovirus isolates compared in this study
Isolates | GenBank accession no. | Host | Origin | Collection Date |
---|---|---|---|---|
GPV-06-0329 (41) | EU583391.1 | Goose | Taiwan, China | 2006 |
GPV-VG32/1 (42) | EU583392.1 | Goose | Germany | 2004 |
GPV-MDE | MF438102.1 | Mule duck | Fujian, China | 2015 |
GPV-RC16 | KY475562.1 | Goose | Chongqing, China | 2016 |
GPV-E (61) | KC184133.1 | Goose | Anhui, China | 2012 |
GPV-B (48) | U25749.1 | Hungary | 1995 | |
GPV-G7 (47) | KR029617.1 | Muscovy duck | Fujian, China | 2013 |
GPV-HuN18 (61) | MK736656.1 | Linwu sheldrake | Fujian, China | 2018 |
GPV-GER (39) | KU684472.1 | Ornamental duck | Poland | 2015 |
GPV-GD | MH444514.1 | Mule duck | China | 2016 |
NGPV-DS15 (21) | KX384726.2 | Cherry Valley duck | Anhui, China | 2015 |
NGPV-SDLY1602 (23) | MF441222.1 | Cherry Valley duck | Shangdong, China | 2016 |
NGPV-sdlc01 (4) | KT343253.1 | Cherry Valley duck | Fujian, China | 2015 |
NGPV-SDHZ1604 (4) | MF441223.1 | Cherry Valley duck | Shangdong, China | 2016 |
NGPV-SDLY1512 (4) | MF441221.1 | Cherry Valley duck | Shangdong, China | 2015 |
NGPV- JS1603 (23) | MF441226.1 | Cherry Valley duck | Jiangsu,China | 2016 |
NGPV-SC16 | KY679174.1 | Cherry Valley duck | Sichuan, China | 2016 |
NGPV-QH15 | KT751090.1 | Peking duck | China | 2015 |
NGPV-AH1606 (23) | MF441225.1 | Cherry Valley duck | Anhui, China | 2016 |
NGPV-SDDY1605 (23) | MF441224.1 | Cherry Valley duck | Shangdong, China | 2016 |
MDPV-FJV1 | KR029616.1 | Muscovy duck | China | 2011 |
MDPV-GX5 (56) | KM093740.1 | Muscovy duck | Guangxi, China | 2011 |
MDPV-ZW (16) | KY744743.1 | Muscovy duck | China | 2006 |
MDPV-JH06 (50) | MH807697.1 | Muscovy duck | Zhejiang, China | 2006 |
MDPV-FJM2 | KR075688.1 | Muscovy duck | China | 2013 |
MDPV-SAAS-SHNH | KC171936.1 | Muscovy duck | Shanghai, China | 2012 |
MDPV-M8 | KR029614.1 | Muscovy duck | Fujian, China | 2013 |
MDPV-GDNX (10) | MH204100.1 | Muscovy duck | Guangdong, China | 2016 |
MDPV-JH10 (50) | MH807698.1 | Muscovy duck | Zhejiang, China | 2010 |
MDPV-YL08 | MG932366.1 | Muscovy duck | China | 2008 |
After genetic comparison, the characteristic variable region of the GPV NS gene is obviously different from that of MDPV. The TaqMan real-time PCR method developed can effectively distinguish GPV and MDPV, and a specific detection method for GPV and MDPV is established thereby. The results of real-time PCR showed that 21 of the 37 GPV and NGPV strains share the sequence of AGAGAAGCA GGAACAATTACCAGGT and these 21 sequences belong to the GPV group. Twelve of the 37 sequences share the codon for AGAGAAGCAGGAACAATT ACCAGGT and 12 sequences belong to the NGPV group. Two probes were designed and both can be used to quantify GPV and NGPV and to distinguish between these two viruses (46).
In this review, we selected full-length sequences of 30 strains of GPV, MDPV and NGPV. The results of the phylogenetic analysis are shown in Fig. 2. It was found that NGPV has a high degree of genetic identity with GPV. The genetic identity between the 10 strains of MDPV was higher at approximately 97%, but their genetic identity with GPV and NGPV was lower. The genetic identity of GPV-VG3/1 from Germany with the GPV-B strain from Hungary reached 98%, indicating that the German strain may have been transported into the country
GPV, MDPV and NGPV are three waterfowl infectious diseases that cause Derzsy’s disease, Muscovy duck parvovirus disease and duck short beak and dwarfism syndrome, respectively. The pathogens pose a serious threat to the development of waterfowl farming worldwide. The clinical symptoms of the infectious diseases caused by GPV and Muscovy parvovirus are similar, including loss of appetite and difficulty in breathing, and with both there are high mortality and high morbidity. In recent years, the duck short beak and dwarfism syndrome caused by a new variant of GPV (NGPV) has been incident at 60%, and although the mortality rate has not been very high, the weight gain by stunting has caused serious economic losses to the Chinese aquatic poultry industry.
The genomes and amino acids of these three viruses are highly homologous, so the genetic relationship between the three parvoviruses has attracted great interest from researchers. In recent years, many research institutes and universities have made major breakthroughs in the identification of the three parvoviruses and the differences from other parvoviruses, but the pathogenic mechanism and evolution process of GPV, MDPV, and NGPV and the full functions of structural and non-structural proteins at present are still unclear and further work should be carried out. Since the