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Viral hepatitis in poultry is a complex disease syndrome caused by several viruses belonging to different families including avian hepatitis E virus (HEV), duck hepatitis B virus (DHBV), duck hepatitis A virus (DHAV-1, -2, -3), duck hepatitis virus Types 2 and 3, fowl adenoviruses (FAdV), and turkey hepatitis virus (THV). While these hepatitis viruses share the same target organ, the liver, they each possess unique clinical and biological features. In this article, we aim to review the common and unique features of major poultry hepatitis viruses in an effort to identify the knowledge gaps and aid the prevention and control of poultry viral hepatitis. Avian HEV is an Orthohepevirus B in the family Hepeviridae that naturally infects chickens and consists of three distinct genotypes worldwide. Avian HEV is associated with hepatitis-splenomegaly syndrome or big liver and spleen disease in chickens, although the majority of the infected birds are subclinical. Avihepadnaviruses in the family of Hepadnaviridae have been isolated from ducks, snow geese, white storks, grey herons, cranes, and parrots. DHBV evolved with the host as a noncytopathic form without clinical signs and rarely progressed to chronicity. The outcome for DHBV infection varies by the host's ability to elicit an immune response and is dose and age dependent in ducks, thus mimicking the pathogenesis of human hepatitis B virus (HBV) infections and providing an excellent animal model for human HBV. DHAV is a picornavirus that causes a highly contagious virus infection in ducks with up to 100% flock mortality in ducklings under 6 wk of age, while older birds remain unaffected. The high morbidity and mortality has an economic impact on intensive duck production farming. Duck hepatitis virus Types 2 and 3 are astroviruses in the family of Astroviridae with similarity phylogenetically to turkey astroviruses, implicating the potential for cross-species infections between strains. Duck astrovirus (DAstV) causes acute, fatal infections in ducklings with a rapid decline within 1–2 hr and clinical and pathologic signs virtually indistinguishable from DHAV. DAstV-1 has only been recognized in the United Kingdom and recently in China, while DAstV-2 has been reported in ducks in the United States. FAdV, the causative agent of inclusion body hepatitis, is a Group I avian adenovirus in the genus Aviadenovirus. The affected birds have a swollen, friable, and discolored liver, sometimes with necrotic or hemorrhagic foci. Histologic lesions include multifocal necrosis of hepatocytes and acute hepatitis with intranuclear inclusion bodies in the nuclei of the hepatocytes. THV is a picornavirus that is likely the causative agent of turkey viral hepatitis. Currently there are more questions than answers about THV, and the pathogenesis and clinical impacts remain largely unknown. Future research in viral hepatic diseases of poultry is warranted to develop specific diagnostic assays, identify suitable cell culture systems for virus propagation, and develop effective vaccines.

Fowl adenovirus (FAdV) has caused significant losses in chicken flocks throughout China in recent years. However, the current understanding of the genetic and pathogenic characteristics of the FAdV epidemic in southwestern China remains poorly understood. In this study, a total of 22 strains were isolated from liver samples of diseased chickens from farms in southwestern China. Phylogenetic analysis based on the hexon loop-1 gene showed that the 22 isolates were clustered into four distinct serotypes: FAdV serotype 4 (FAdV-4) (86.4%, 19/22), FAdV-2 (4.5%, 1/22), FAdV-8a (4.5%, 1/22), and FAdV-8b (4.5%, 1/22). FAdV-4 was the predominant serotype in southwestern China. Pathogenicity testing showed that the FAdV-4 serotype strain CH/GZXF/1602 and FAdV-8a strain CH/CQBS/1504 were pathogenic to chickens, with mortality rates reaching as high as 80% and 20%, respectively. The primary clinical feature observed following infection with strain CH/GZXF/1602 (FAdV-4) was hepatitis-hydropericardium syndrome, and that of strain CH/CQBS/1504 (FAdV-8a) was inclusion body hepatitis. Conversely, the FAdV-2 serotype strain CH/GZXF/1511 and FAdV-8b serotype strain CH/CQBS/1512 was not observed to be pathogenic in chickens. Then, CH/GZXF/1602 (FAdV-4) was selected for the preparation of an inactivated oil-emulsion vaccine. Immune studies on Partridge Shank broilers showed that a single dose immunization at 17 days of age could not only protect against homologous challenge with virulent FAdV-4 but also provided protection against clinical disease following challenge with the heterologous FAdV-8b virulent strain until 70 days of age. The characterization of newly prevalent FAdV strains provides a valuable reference for the development of an efficacious control strategy. Emerging Microbes & Infections (2017) 6, e103; doi: 10.1038/emi.2017.91 ; published online 29 November 2017

Fowl adenoviruses (FAdVs) are distributed worldwide in poultry and incriminated as the etiological agents for several health problems in fowls, and are capable of crossing species barriers between domestic and wild fowls. An FAdV strain was, for the first time, isolated from black-necked crane in this study, and was designated as serotype 4 Fowl aviadenovirus C (abbreviated as BNC2021) according to the phylogenetic analysis of its DNA polymerase and hexon gene. The viral genomic sequence analysis demonstrated that the isolate possessed the ORF deletions that are present in FAdV4 strains circulating in poultry fowls in China and the amino acid mutations associated with viral pathogenicity in the hexon and fiber 2 proteins. A viral challenge experiment with mallard ducks demonstrated systemic viral infection and horizontal transmission. BNC2021 induced the typical clinical signs of hepatitis–hydropericardium syndrome (HHS) with swelling and inflammation in multiple organs and showed significant viral replication in all eight organs tested in the virus-inoculated ducks and their contactees at 6 dpi. The findings highlight the importance of surveillance of FAdVs in wild birds.

Single or mixed infections of multiple pathogens such as avian hepatitis E virus (aHEV) and avian leukosis virus subgroup J (ALV-J) have been detected in numerous laying hens with severe liver injury in China. Thus, aHEV and immunosuppressive viruses are speculated to cause co-infections. In this study, co-infection with aHEV and fowl adenovirus (FAdV) was confirmed by nested RT-PCR and recombinase-aided amplification combined with gene sequencing in two flocks with severe liver injury. Subsequently, the two reference strains, aHEV and FAdV-4, were inoculated into LMH cells to identify their co-infection potential. Confocal microscopy revealed aHEV and FAdV-4 co-infected LMH cells. In addition, the replication dynamics of aHEV and FAdV-4 along with the expression levels of immuno-cytokines were measured. The results indicated colocalization of aHEV and FAdV-4 and inhibition of viral replication in LMH cells. The transcription levels of MDA5, Mx, OASL, and IFN-α were significantly upregulated in LMH cells, whereas those of immune-related factors induced by FAdV-4 were downregulated upon FAdV-4 and aHEV co-infection. These results confirmed the co-infection of aHEV and FAdV-4 in vitro and prompted the antagonistic pathogenic effects of FAdV-4 and aHEV, thereby providing novel insights into the counterbalancing effects of these viruses.

Fatty acids (FAs) are important precursors of oolong tea volatile substances, and their famous derivatives have been shown to be the key aroma components. However, the relationship between fatty acids and their derivatives during oolong tea production remains unclear. In this study, fresh Tieguanyin leaves were manufactured into oolong tea and green tea (control), and fatty acids and fatty acid-derived volatiles (FADV) were extracted from processed samples by the sulfuric acid–methanol method and solvent-assisted flavor evaporation (SAFE), respectively. The results showed that unsaturated fatty acids were more abundant than saturated fatty acids in fresh leaves and decreased significantly during tea making. Relative to that in green tea, fatty acids showed larger variations in oolong tea, especially at the green-making stage. Unlike fatty acids, the FADV content first increased and then decreased. During oolong tea manufacture, FADV contents were significantly and negatively correlated with total fatty acids; during the green-making stage, methyl jasmonate (MeJA) content was significantly and negatively correlated with abundant fatty acids except steric acid. Our data suggest that the aroma quality of oolong tea can be improved by manipulating fatty acid transformation.

Adenoviral pancreatitis has been amply described for decades in guinea fowl. Although its pathologic picture has been characterized fairly well, its etiology still remains only partially clarified. Based on several outbreaks diagnosed on commercial guinea flocks raised in France since 2017, we performed direct whole-genome sequencing from pancreatic lesional tissue by using the Oxford Nanopore Technologies (ONT) sequencing method. We generated 4781 viral reads and assembled a whole genome of 43,509 bp, clustering within fowl adenovirus type 1 (FAdV-1). A phylogenetic analysis based on a partial sequence of the hexon and short fiber genes on viruses collected in France showed 98.7% and 99.8% nucleotide identity, respectively. Altogether, these results confirm that an FAdV-1 closely related to chicken and other avian strains is the agent of pancreatitis in guinea fowl. This study illustrates the potential of ONT sequencing method to achieve rapid whole-genome sequencing directly from pathologic material.

Fowl aviadenovirus (FAdV) is an important pathogen in the global poultry industry and the etiology of inclusion body hepatitis-hydropericardium syndrome (HHS) in chickens. Since the 1990s, several outbreaks of HHS have occurred in poultry producing areas, including South America. The coinfection of FAdV and chicken anemia virus (CAV) may markedly impact the incidence of HHS. This study describes an outbreak of HHS in coinfection with CAV in industrial broiler breeders and characterizes the FAdV isolate. The three-week-old male broiler breeders had pale bone marrow, enlarged and yellowish liver, splenomegaly, and atrophied thymus; one chicken was also found with hydropericardium. Virus isolation was performed in SPF chicken embryos of liver and thymus. Tissues of the naturally infected chickens and the inoculated embryos were evaluated by PCR and histopathology. All affected chickens and inoculated embryos were positive for FAdV and CAV. The inoculated embryos had enlarged, greenish and hemorrhagic livers, and 30% died within 7 days of inoculation. Phylogenetic analysis of the FAdV isolate hexon gene partial sequence enabled grouping with E species. The E species has recently become a relevant species in several countries. The association of FAdV with CAV in breeders is of further concern due to both being capable of vertical transmission. Within the last decade, a worldwide upsurge of HHS in broiler breeders owing to failed biosecurity has occurred. In this episode, the failure on biosecurity may have enabled challenge with both FAdV and CAV, with pathological synergism. The CAV-impaired adaptive immunity may have benefited the FAdV infection. RESUMO: Adenovírus aviário (FAdV) é um importante patógeno na indústria avícola global e a etiologia da síndrome da hepatite por corpúsculo de inclusão-hidropericárdio (SHH) em galinhas. Desde a década de 1990, vários surtos de SHH foram descritos em todas as áreas de produção de aves, incluindo na América do Sul, e a coinfecção entre FAdV e vírus da anemia das galinhas (CAV) pode ser agravante para todos os aspectos da SHH. Objetiva-se descrever um surto de SHH em matrizes de frangos corte, caracterizar a estirpe de FAdV envolvida e destacar a coinfecção com CAV. Foram avaliados machos reprodutores de corte com três semanas de idade, com medula óssea pálida, fígado aumentado e amarelado e esplenomegalia, timo atrofiado e um com hidropericárdio. Fígado e timo foram coletados para isolamento do vírus em embriões de galinhas SPF, PCR e histopatologia. Todas as aves acometidas e embriões inoculados foram positivos para FAdV e CAV. Os embriões inoculados tiveram óbito de 30% em até sete dias após a inoculação e alterações hepáticas por fígados esverdeados e aumentados. A análise filogenética de FAdV com base em parte da sequência do gene que codifica a proteína hexon revelou identidade com a espécie E, que se tornou disseminada em vários países. A coinfecção de FAdV e CAV resulta em maior intensidade de lesões, maior morbidade e mortalidade e em reprodutores tem alta relevância epidemiológica, em razão da transmissão vertical de ambos e da ampla distribuição geográfica das progênies infectadas. Na última década, ocorreu um aumento mundial na ocorrência de SHH em frangos de corte relacionado a falhas em biosseguridade, especialmente em reprodutores, condição que pode ter ocorrido neste episódio. A presença de FAdV e CAV em reprodutores é motivo para preocupação por reflexos negativos à imunidade e viabilidade das progênies.

Fowl adenoviruses (FAdVs, species FAdV-A/-E) are responsible for several clinical syndromes reported with increasing frequency in poultry farms in the last decades. In the present study, a phylodynamic analysis was performed on a group of FAdV-D Hexon sequences with adequate available metadata. The obtained results demonstrated the long-term circulation of this species, at least several decades before the first identification of the disease. After a period of progressive increase, the viral population showed a high-level circulation from approximately the 1960s to the beginning of the new millennium, mirroring the expansion of intensive poultry production and animal trade. At the same time, strain migration occurred mainly from Europe to other continents, although other among-continent connections were estimated. Thereafter, the viral population declined progressively, likely due to the improved control measures, potentially including the development and application of FAdV vaccines. An increase in the viral evolutionary rate featured this phase. A role of vaccine-induced immunity in shaping viral evolution could thus be hypothesized. Accordingly, several sites of the Hexon, especially those targeted by the host response were proven under a significant pervasive or episodic diversifying selection. The present study results demonstrate the role of intensive poultry production and market globalization in the rise of FAdV. The applied control strategies, on the other hand, were effective in limiting viral circulation and shaping its evolution.

Fowl adenoviruses (FAdVs) are widespread viruses in poultry populations, responsible for several severe diseases, including Inclusion Body Hepatitis (IBH), Adenoviral Gizzard Erosion (AGE), and Hepatitis-Hydropericardium Syndrome (HHP). These diseases have been associated with significant economic and health impacts on poultry industries. Accurate detection and genotyping play a key role in the diagnosis of these infections, as different FAdV genotypes are associated with distinct disease syndromes and epidemiological patterns. In this study, we aimed to evaluate the clinical, analytical, and genotyping performance of the Hex L1 PCR combined with High-Resolution Melting (HRM) Curve analysis for investigating recent IBH and AGE outbreaks in Morocco. The study involved 26 clinical samples collected from broiler and layer poultry farms suspected with IBH or AGE. These samples were amplified using conventional PCR, real-time PCR/52 K test, and the Hex L1 PCR/HRM test. Field samples were also sequenced and compared with HRM curve analysis results to validate the genotyping accuracy of the Hex L1 PCR/HRM method. Phylogenetic analysis of the sequenced samples revealed several FAdV genotypes, including FAdV-11 and FAdV-8b in IBH cases, and FAdV-1 and FAdV-8a in AGE cases, highlighting the genetic diversity of circulating strains. The Hex L1 PCR/HRM method successfully amplified all 12 FAdV serotypes, demonstrating excellent reproducibility and repeatability, with coefficients of variation ranging from 0.19% to 1.82%. Moreover, this method showed a strong correlation with the real-time PCR/52 K test, achieving a high correlation coefficient of 0.9077. The HRM curve analysis accurately genotyped all the field samples, with results consistent with sequencing outcomes. In conclusion, this method provides a fast, sensitive, and reliable alternative for FAdV detection and genotyping. It enables universal detection, quantification, and genotyping in a single step, overcoming the limitations of traditional techniques, making it an ideal tool for sample screening, while sequencing validation is necessary for confirmation.

•Bivalent (FAdV-8b-Sk + FAdV-11-1047) live FAdV is safe as a broiler breeder vaccine.•Live and inactivated bivalent vaccines both induce neutralizing antibodies (NAb).•Transferred MtAb protects the progeny against lethal challenge.•Bivalent live and inactivated FAdV vaccines are equally effective and have the potential for IBH control. Fowl adenovirus (FAdV) is comprised of five species (A to E) and 12 serotypes (1–7, 8a, 8b, 9–11). Inclusion body hepatitis (IBH) is caused by FAdV-7, 8a, 8b (species E) and FAdV-2 and 11 (species D). Commercial vaccines against IBH are not available in Canada. Autogenous FAdV broiler breeder vaccines are now used in some areas where outbreaks of IBH are occurring. The objective of this study was to evaluate the efficacy of a bivalent (species D and E) live and an inactivated FAdV broiler breeder vaccine in protecting broiler chicks against IBH through maternal antibody (MtAb) transfer. FAdV seronegative broiler breeders (n = 300/group) received either a live or inactivated bivalent (FAdV-8b-SK + FAdV-11-1047) vaccine. The live vaccine (1 × 104 TCID50 of each virus/bird) was given orally once at 16 weeks of age and the inactivated vaccine (1 × 106TCID50 of each virus + 20% Emulsigen D) was given intramuscularly at 16 and 19 weeks of age. Controls (n = 150) were given saline orally. The inactivated vaccine group was boosted 3 weeks later with the same vaccine. Neutralizing antibodies (NAb) in sera (n = 10) were detected at 19, 22, 30 and 48 weeks of age. NAb were able to neutralize various FAdV serotypes within species D and E. Mean NAb were similar in the both live and killed vaccine groups at 19, 30 and 48 weeks and ranged from 2.4 to 3.7 log10. Approximately 26 ± 7% of MtAbs were passively transferred through eggs to day-old chicks. Progeny challenged with a lethal dose (1 × 107 TCID50/bird intramuscularly) of FAdV-8b-SK, FAdV-11-1047, or FAdV-2-685 (n = 90/group) at 14 days post-hatch (dph) showed 98–100% protection in broiler chicks to homologous or heterologous FAdV challenges. Our data suggests that a bivalent live and an inactivated FAdV vaccine are equally effective and have the potential for the control of IBH.