Chicken astrovirus

Astroviruses are small, round and 25-35 nm in diameter. Their name originates from the 5- or 6-pointed star-like surface projections observed on their virions using electron microscopy with negative staining. Astroviruses are non-enveloped, positive-sense RNA viruses. Their viral genome is 6.5-7.5 kilobases long and contains three open-reading frames (ORF). These ORFs encode non-structural proteins (ORF1a), a viral RNA-dependent RNA polymerase (ORF1b), and the capsid precursor protein (ORF2). The Astroviridae family is divided into two genera: Mamastrovirus (mammal astroviruses) and Avastrovirus (avian astroviruses). Within each genus, numerous groups have been described based on serotype and genetic differences. The first astrovirus, observed by Appleton and Higgins in Reference APPLETON and HIGGINS1975, was found in association with an outbreak of diarrhoea and vomiting in a maternity ward in England. In the 1960s a viral disease was described in ducks (Asplin, Reference ASPLIN1965), and the viral agent was identified in 1984 as an astrovirus (Schultz-Cherry et al., Reference SCHULTZ-CHERRY, KING and KOCI2001).

Astroviruses have been associated with enteric disease in humans and young animals, such as calves, lambs, pigs, dogs, cats, and mink (Maondez and Arias, Reference MAONDEZ and ARIAS2007). In poultry, five avian astroviruses (AAstVs) have been identified: turkey astrovirus (TAstV-1, TAstV-2), avian nephritis virus (ANV, G-4260), chicken (CAstV), and duck astrovirus (DAstV). Chicken astrovirus has been detected in chicks with runting-stunting syndrome (RSS). Various astroviruses have been found in young turkeys and chickens with enteritis and increased mortality. Astroviruses have been isolated from the intestines of birds affected with viral enteric diseases (Pantin-Jackwood et al., Reference PANTIN-JACKWOOD, DAY, JACKWOOD and SPACKMAN2008). Clinical signs of disease develop at between one and three weeks of age, and include diarrhoea, decreased feed consumption and nervous behaviour (Pantin-Jackwood et al., Reference PANTIN-JACKWOOD, SPACKMAN and WOOLCOCK2006; Reynolds and Schultz-Cherry, Reference REYNOLDS and SCHULTZ-CHERRY2008; Kang et al., Reference KANG, EL-GAZZAR, SELLERS, DOREA, WILLIAMS, KIM, COLLETT and MUNDT2012). The diarrhoea produced by astrovirus has been attributed to the osmotic effect promoted by the disaccharides and other non-digested and non-absorbed nutrients that attract water to the gut interior, destroy the intestinal mucosa, and produce alterations in ionic channels (Moser and Schultz-Cherry, Reference MOSER and SCHULTZ-CHERRY2005).

Avian astroviruses replicate principally in the intestine, producing viremia, thymic depression, and decreasing the number of lymphocytes in the peripheral blood system. Unlike with other enteric viruses, astrovirus infection does not induce the alteration of intestinal villi. Astrovirus was identified in the cytoplasm of the intestinal epithelial cells, located to the sides and the bottom of intestinal villi, and viral release into the intestinal lumen occur as a consequence of the degeneration of enterocytes (Reynolds and Schultz-Cherry, Reference REYNOLDS and SCHULTZ-CHERRY2008).

Historically, electron microscopy has been the primary method for diagnosis. With the passage of time, other methods that are easier, quicker, more sensitive and specific have been developed. For example, to accomplish antibody detection, assays such as ELISA have been used. In addition, molecular methods, using techniques such as reverse transcription polymerase chain reaction (RT-PCR), have been used to detect these viral agents in animals (Baxendale and Mebatsion, Reference BAXENDALE and MEBATSION2004; De Wit et al., Reference DE WIT, DAM, DE LAAR, BIERMANN, VERSTEGEN, EDENS and SCHRIER2011).

Avian nephritis virus (ANV)

Avian nephritis virus (ANV) produces an acute disease that is highly contagious and characterised by kidney alterations in birds, principally in the young. This virus is classified within a new genus of the family Astroviridae (Imada et al., Reference IMADA, YAMAGUCHI, MASE, TSUKAMOTO, KUBO and MOROOKA2000). The avian nephritis virus is a non-enveloped, positive-sense RNA virus. Avian nephritis virus is small, round, approximately 28 nm in diameter and possesses a genome of positive-sense RNA, along with an icosahedral capsid. Its genome contains approximately 7,000 nucleotides (nt), with three open reading frames (ORF): ORF 1a, 1b and 2. ORF 1 codes for a protease called 3C. ORF1b codes for a viral RNA-dependent RNA polymerase and ribosomal structure localised between the two ORFs (ORF 1a and ORF 1b). ORF2 codes for the lipoprotein precursors of the capsid (Zhao et al., Reference ZHAO, ZHU, YU, YUAN, ZHU, YANG, CUI and HUA2011).

ANV was first isolated in 1976 in Japan from the rectal content of seeming healthy one-week-old chickens. It was found in chicken embryo kidney cell cultures, and identified as a picornavirus. ANV was previously classified as a member of genus Enterovirus, family Picornaviridae, because of its physico-chemical and morphological properties. Many experimental studies have indicated that the target organ of the virus could be the kidney; thus, it was proposed that the virus should be called avian nephritis virus, a name that has endured (Imada et al., Reference IMADA, YAMAGUCHI and KAWAMURA1979; Reference IMADA, TANIGUCHI, YAMAGUCHI, MINETOMA, MAEDA and KAWAMURA1981; Reference IMADA, YAMAGUCHI, MASE, TSUKAMOTO, KUBO and MOROOKA2000). After ANV was isolated from chickens, it was re-classified as an astrovirus following the complete sequencing of the viral genome (Imada et al., Reference IMADA, YAMAGUCHI, MASE, TSUKAMOTO, KUBO and MOROOKA2000). More specifically, avian nephritis virus has been classified as a new member of the family Astroviridae. Recently, comparative analysis of the capsid genes revealed extensive genetic variation among AAstVs and the presence of the distinct genotypes (TAstV-1, TAstV-2, ANV and CAstV) in poultry (Pantin-Jackwood et al., Reference PANTIN-JACKWOOD, STROTHER, MUNDT, ZSAK, DAY and SPACKMAN2011).

Studies of pathogenicity have determined that diarrhoea and nephrosis occur three to six days post-inoculation. Death due to visceral deposition of urates occurs seven days post-inoculation (Shirai et al., Reference SHIRAI, NAKAMURA, SHINOHARA and KAWAMURA1991). In addition, the wild-type virus may present different stages of pathogenicity in chickens, suggesting that serotypes and strains may vary in their capacity to cause disease and death (Hewson et al., Reference HEWSON, O'ROURKE and NOORMOHAMMADI2010). This virus principally affects young birds that later develop clinical disease and kidney lesions, tubule nephrosis, interstitial nephritis and death. In addition, ANV has also been associated with diarrhoea, stunting and death in chicks or young birds (Imada et al., Reference IMADA, TANIGUCHI, YAMAGUCHI, MINETOMA, MAEDA and KAWAMURA1981; Reference IMADA, YAMAGUCHI and KAWAMURA1979). Many studies have detected ANV in the intestinal contents of flocks of broiler chickens affected with retardation of growth (Todd et al., Reference TODD, TRUDGETT, MCNEILLY, MCBRIDE, DONNELLY, SMYTH, JEWHURST and ADAIR2010).

The diagnosis of avian nephritis virus is conducted using electron microscopy, immuno-enzymatic methods to detect immunoglobulin and via molecular techniques, the latter which have led to increased speed, specificity and sensitivity of virus detection. Molecular techniques such as RT-PCR and genetic sequencing have been developed and used for both diagnosis and molecular characterisation of ANV (Day et al., Reference DAY, SPACKMAN and PANTIN-JACKWOOD2007; Todd et al., Reference TODD, TRUDGETT, MCNEILLY, MCBRIDE, DONNELLY, SMYTH, JEWHURST and ADAIR2010; Zhao et al., Reference ZHAO, ZHU, YU, YUAN, ZHU, YANG, CUI and HUA2011). These techniques have allowed the verification of the virus circulating in the United States, Australia, Japan, China, Hungary and Brazil in commercial flocks of chickens and turkeys that are otherwise apparently normal or showing signs of enteric diseases, such as diarrhoea (Hewson et al., Reference HEWSON, O'ROURKE and NOORMOHAMMADI2010; Todd et al., Reference TODD, TRUDGETT, MCNEILLY, MCBRIDE, DONNELLY, SMYTH, JEWHURST and ADAIR2010; Bidin et al., Reference BIDIN, LOJKIĆ, BIDIN, TISLJAR, MAJNARIĆ and MIKEC2011; Zhao et al., Reference ZHAO, ZHU, YU, YUAN, ZHU, YANG, CUI and HUA2011).

Chicken parvovirus

Chicken parvovirus is related to enteric disease in chickens, principally causing growth retardation, decreased weight gain and diarrhoea. Parvoviruses are small and non-enveloped viruses with a straight simple chain of DNA and a 5-kb genome. The viruses have a non-enveloped capsid of hexagonal shape with 32 capsomeres that are 20-22 nm in diameter. The capsid has icosahedral symmetry formed of two to four superimposed proteins, called VP1-VP4 (Hueffer and Parrish, Reference HUEFFER and PARRISH2003). The VP2 protein is the larger structural protein and is detected in high concentrations on the capsid surface. This protein is associated with host and tissue tropism and the fusion of the cellular receptor and the epitopes that bind to antibodies. The N-terminal sequence from this protein is exported through a channel, which leads to the protein being cleaved and producing VP3 protein. The N-terminal is also used for DNA packaging that leaves sequences from the end of the genome exposed on the outside of the capsid. Other features of the capsid in parvoviruses of vertebrates may include one large or three smaller spike-like protrusions surrounding the icosahedral threefold axes of symmetry, depressions around the fivefold axes, and dimple-like depressions at the icosahedral twofold axes, where antibodies are bound (Berns and Parrish, Reference BERNS and PARRISH2007). The family Parvoviridae contains two subfamilies: Parvovirinae, that infects vertebrates, and Desovirinae, that infects insect and other invertebrates (Berns and Parrish, Reference BERNS and PARRISH2007).

Chicken parvovirus was first described by Kisary et al. (Reference KISARY, NAGY and BITAY1984). Small viral particles were detected by electron microscopy in samples of intestinal contents of 10-day-old chickens. These particles were 19-24 nm in diameter, with hexagonal symmetry. Kisary et al. (Reference KISARY, NAGY and BITAY1984) suggested that this virus could be involved with RSS as these birds demonstrated pronounced growth retardation, poor feathering and extremely pale intestines (Kisary et al., Reference KISARY, NAGY and BITAY1984).

In 1985, Kisary and co-workers suggested that this newly recognised virus be classified as fowl parvovirus due to the morphology, size and buoyant density of the virions, as well as its genomic structure. Experimental infections in 1-day-old chickens indicated that fowl parvovirus in broiler chicks may play an important role in decreasing their growth rate below expected levels. Experimental infections in chicken embryos indicated that infected chicks were poorly developed leading to low vitality and early chick mortality (Kisary et al., Reference KISARY, AVALOSSE, MILLER-FAURES and ROMMELAERE1985).

The replication of parvovirus depends on cellular factors that are present during the S phase of the cell cycle. Thus, the replication and pathogenic effects predominate in cells with high levels of cell proliferation. Intestinal disease occurs as a result of parvovirus infection in epithelial cells in Liberkuhn's crypts (Guy, Reference GUY1998).

The viral diagnosis of parvovirus is conducted with electron microscopy, indirect immune-fluorescence, immuno-enzymatic techniques (ELISA) and molecular techniques (PCR and Real Time PCR), that increase the specificity and sensitivity of the diagnosis (Zsak et al., Reference ZSAK, STROTHER and KISARY2008; Reference ZSAK, STROTHER, DAY and STROTHER2009; Strother and Zsak, Reference STROTHER and ZSAK2009; Tarasiuk et al., Reference TARASIUK, WOŹNIAKOWSKI and SAMOREK-SALAMONOWICZ2012).

Chicken parvovirus and turkey parvovirus were detected in the intestinal samples of enteritis-affected poultry, suggesting that both viruses play a role in the etiology of enteric diseases in poultry, principally in RSS and poult enteritis complex (PEC) (Zsak et al., Reference ZSAK, STROTHER and KISARY2008).

Fowl adenovirus group 1

Fowl adenoviruses (FAdVs) of group 1 form in chickens are associated with inclusion body hepatitis (IBH), hydropericardium syndrome (HPS), gizzard erosions, ventriculitis, proventriculitis, enteritis and RSS (Fitzgerald, Reference FITZGERALD2008). Adenoviruses are DNA viruses with an icosahedral structure, measuring 70-90 nm in diameter. The virion is enveloped with a double chain of DNA that corresponds to 11.3-13.5% of the virion. The virion is composed of 252 capsomeres. The capsomeres are triangular in shape. There are 240 capsomeres that are not part of the vertices (hexones) of the triangles in the virion. They are 8-9.5 mm in diameter, and there are 12 capsomeres for each vertex (pentonic bases). The capsomeres of the vertices have projections known as fibres. Avian adenovirus has two fibres for each pentonic base; a distinguishing characteristic from the mammal adenovirus, that has only one fibre for each pentonic base (Berk, Reference BERK2007).

Adenoviruses are in the family Adenoviridae and are grouped into five genera Aviadenovirus. The genus Aviadenovirus currently comprises five fowl FAdVs (fowl adenovirus A-E), a falcon (Falcon adenovirus A) and a goose adenovirus (Goose adenovirus) species (Grgić et al., Reference GRGIĆ, YANG and NAGY2011).

Adenoviruses are common infectious agents of poultry, although most infections result in subclinical presentation or are associated with mild clinical signs. However, some avian adenovirus strains are associated with a variety of diseases, such as inclusion body hepatitis (IBH), especially serotypes 2, 4, 7, 8 and 11; the disease that has been identified in almost every part of the world (Ojkic et al., Reference OJKIC, MARTIN, SWINTON, VAILLANCOURT, BOULIANNE and GOMIS2008). In addition, respiratory disease and tenosynovitis in chickens have been associated with FAdVs, and a pathogenic role of FAdV-1 in gizzard erosions has also been demonstrated (Ono et al., Reference ONO, OKUDA, SHIBATA, SATO and OKADA2007). However, the role of most subgroup 1 avian adenoviruses as pathogens has not been not well defined. FAdVs are easily transmitted both horizontally and vertically. The first fowl adenovirus isolated from a sick bird was from an outbreak of respiratory diseases in quails (Colinus virsginianus) (Berk, Reference BERK2007; Fitzgerald, Reference FITZGERALD2008).

In addition to the above mentioned specific diseases caused by FAdVs, there have been reports of adenovirus infection resulting in decreased food consumption (Bányai et al., Reference BÁNYAI, KISFALI, BOGDÁN, MARTELLA, MELEGH, ERDMAN and SZUCS2009). Although birds inoculated with adenovirus may have depressed body weight and even high mortality, there is a little evidence to suggest that this naturally occurring infection causes either reduced food utilisation or poor growth. Outside of the liver, the principal replication locations of FAdV group 1 are the digestive tract and superior respiratory tract. The virus frequently is found in the pharynx and kidneys. Experimental studies with inoculated hens have demonstrated decreased feed consumption, loss of body weight, excessive fat accumulation, and high mortality (Toro et al., Reference TORO, PRUSAS, RAUE, CERDA, GEISSE, GONZÁLEZ and HESS1999; Ojkic et al., Reference OJKIC, MARTIN, SWINTON, VAILLANCOURT, BOULIANNE and GOMIS2008).

Fowl adenovirus group 1 has been found in chicks with proventriculitis, stunting and affected feed conversion. Macroscopically, the FAdV-infected chick has a swollen proventriculus with necrotic material or haemorrhages covering the mucosa. Fowl adenovirus group 1 infection may result in proventriculitis, developmental alterations, decreased growth rate and decreased food conversion (Fitzgerald, Reference FITZGERALD2008).

Both conventional and molecular techniques are used for the diagnosis of FAdV related disease. The FAdVs can be detected on the basis of virus isolation in chicken embryos, indirect immuno-fluorescent assay, enzyme linked immunosorbent assay and double immunodiffusion. These conventional methods may not provide accurate information about the serotypes involved. Molecular techniques like polymerase chain reaction (PCR) followed by restriction enzyme analysis (REA) and sequencing have been used for the rapid detection and differentiation of FAdVs (Ojkic et al., Reference OJKIC, MARTIN, SWINTON, VAILLANCOURT, BOULIANNE and GOMIS2008; Alemnesh et al., Reference ALEMNESH, HAIR-BEJO, AINI and OMAR2010).

Infectious bronchitis virus

Avian coronavirus causes enteric, respiratory and renal disease. In young and growing hens, this virus causes respiratory diseases, resulting in loss of body weight and low feed consumption. Other manifestations of infectious bronchitis virus (IBV) include decreased egg production, typical respiratory disease and kidney damage (Cavanagh and Gelb, Reference CAVANAGH and GELB2008).

The IBV is round with pleomorphic features. The envelope is approximately 120 nm in diameter, with many claviform surface projections (spicules). This virus contains three large structures that form part of the virion: the spike glycoproteins (S) and membrane (M), the internal nucleoprotein (N) and the small membrane protein (E). These are essential for viral formation. The glycoprotein S includes glycopeptides S1 and S2 and is related to the inhibition of haemagglutination and viral-neutralisation antibodies. The virus has a single-stranded, positive-sense RNA genome with approximately 27,600 nucleotides. Viral replication is intra-cytoplasmatic and without body inclusion formation (Guy, Reference GUY1998; Reference GUY2008).

IBV is a member of the Coronaviridae family that includes two genera, Coronavirus and Torovirus. The IBV belongs to group three of the genus Coronavirus, along with coronaviruses from other avian species. Groups one and two of the genus Coronavirus include mammal coronaviruses. Coronaviruses are RNA viruses that infect a wide variety of birds and mammals. Infectious bronchitis was first observed in chickens in the United States in North Dakota in 1930. Clinical signs and preliminary studies in 1931 provided the first description of infectious bronchitis (Cavanagh and Gelb, Reference CAVANAGH and GELB2008).

In poultry, IBV and turkey coronavirus (TCoV) have been associated with respiratory and enteric diseases in chickens and turkeys, respectively (González et al., Reference GONZÁLEZ, GOMEZ-PUERTAS, CAVANAGH, GORBALENYA and ENJUANES2003).

Animal infection with IBV typically begins via a respiratory route. However, due to strain tropism, it may begin in other organs (the kidneys, gonads, and intestines). Viral replication produces lesions in several types of epithelial cells, such as cells in the trachea, Harderian gland, lungs, air sacs, kidneys and gonads (oviduct and testicles) (Cavanagh, Reference CAVANAGH2005; Cavanagh and Gelb, Reference CAVANAGH and GELB2008).

Avian infectious bronchitis mainly affects the respiratory, reproductive, and occasionally the renal systems of broilers, layer, and breeder chickens, causing severe economic losses to the poultry industry; however, the implications of IBV infection in the enteric tract remain unknown (Villarreal et al., Reference VILLARREAL, BRANDÃO, CHACÓN, SAIDENBERG, ASSAYAG, JONES and FERREIRA2007).The virus grows in many cells of the digestive tract, such as the oesophagus, proventriculus, duodenum, jejunum, bursa of Fabricius, caecal tonsils, rectum and cloaca, frequently with few pathobiological clinical effects (Cavanagh, Reference CAVANAGH2007). IBV was identified by UTR gene amplification using RT-PCR in commercial flocks with enteric problems and pheasants, peacocks, partridges and quails. Molecular tests are important for diagnosis of IBV (Cavanagh et al., Reference CAVANAGH, MAWDITT, WELCHMAN, BRITTON and GOUGH2002; Bunger et al., Reference BUNGER, CHACÓN, JONES and FERREIRA2009).

Avian rotavirus

Avian rotavirus causes enteric disease in a wide variety of avian species. Avian rotavirus is a spherical, icosahedral, non-enveloped virus 75 nm in diameter that has an RNA genome. The virus belong the genus Rotavirus of the Reoviridae family. This family contains twelve genera that infect vertebrates, invertebrates, plants and fungi (Estes and Kapikian, Reference ESTES and KAPIKIAN2007).

Intact rotavirus virions visualised by negative contrast electron microscopy resemble a wheel with short spokes; thus, the name rotavirus is derived from the Latin word rota, which means wheel. Rotavirus particles have a triple-layered icosahedral protein capsid and a genome made up of 11 segments of double-stranded RNA coding for 6 structural (VP1–4, VP6 and VP7) and 5 non-structural (NSP1–5) proteins. VP6, the major structural protein, forms the middle layer of the triple-layered concentric protein capsid coat. Each segment of RNA consists of an open reading frame (ORF) that codes a protein. Three polypeptide chains denominated VP1, VP2, and VP6 are associated with particles that form the outer core. The proteins VP3, VP4, VP5 and VP7 form the external capsid. The cleavage of VP4 produces VP5 and VP8 and increases viral infectivity. Viral replication occurs in the cytoplasm in vivo. Mature viral particles are released within dilated cisterns of rough endoplasmic reticulum, gaining an envelope during this process (Prasad et al., Reference PRASAD, WANG, CLERX and CHIU1988; Buragohain et al., Reference BURAGOHAIN, CHERIAN, PRABHAKAR and CHITAMBAR2008).

Rotavirus in avian species was first reported by Bergeland et al. (Reference BERGELAND, McANDARAGH and STOTZ1977) who found particles morphologically indistinguishable from rotaviruses in poultry presenting intestinal content with watery droppings and increased mortality.

Rotaviruses of groups A, D, F and G have been detected in different avian species, but their causative role in diarrhoea and the chronic disease designated as RSS is not completely understood. Group A rotaviruses have been reported causing diarrhoea in children and young animals of many species of birds and mammals (Day et al., Reference DAY, SPACKMAN and PANTIN-JACKWOOD2007).

The diarrhoea associated with rotavirus infection has been attributed to decreased absorption in the intestinal tract of D-xylose and other carbohydrates, such as glucose, that possibly permit bacterial fermentation that produces metabolic products that attract water into the intestinal tract, resulting in diarrhoea (McNulty and Reynolds, Reference MCNULTY and REYNOLDS2008).

Rotavirus has been isolated from many avian species, including ducks, pheasants, chickens, turkeys, and wild birds. In chickens, symptoms related to rotavirus range from subclinical diarrhoea with growth retardation to increased mortality. Researchers have suggested many others viruses, including rotavirus, as potential causes of, or cofactors in, RSS (Otto et al., Reference OTTO, LIEBLER-TENORIO, ELSCHNER, REETZ, LÖHREN and DILLER2006).

Avian rotavirus from hens has been associated with enteric disturbance, which is characterised by runting and signs such as diarrhoea, poor or abnormal appetite, gaseous enteric contents or abnormal fluids and increased mortality. Avian rotavirus is distributed around the world. It is shed through faeces, with horizontal transmission thought to be the most important via of spread. Thus, diagnosis by serological tests may not be wholly effective, necessitating molecular assays, such as RT-PCR (Pantin-Jackwood et al., Reference PANTIN-JACKWOOD, DAY, JACKWOOD and SPACKMAN2008).

Avian reovirus

Avian orthoreoviruses (ARVs) are responsible for considerable economic losses to the poultry industry. Reoviruses have been isolated from a variety of tissues in chickens affected by disease conditions, including viral arthritis/tenosynovitis, stunting syndrome, respiratory disease, enteric disease, immunosuppression, and malabsorption syndrome (Bányai et al., Reference BÁNYAI, DANDÁR, DORSEY, MATÓ and PALYA2011).

Avian reoviruses are fusogenic viruses that belong to the genus Orthoreovirus; one of the twelve genera of the Reoviridae family. Avian reovirus is a RNA virus that replicates in the cytoplasm within cytoplasmic globule inclusions termed viral factories. These structures contain viral structural and non-structural proteins together with viral RNA. ARV is one of the few non-enveloped viruses able to induce fusion of infected cells (Tourís-Otero et al., Reference TOURÍS-OTERO, CORTEZ-SAN MARTÍN, MARTÍNEZ-COSTAS and BENAVENTE2004).

The virion is an icosahedral, multilayered, non-enveloped particle with a diameter of 70-80 nm. The genome comprises ten of double-stranded RNA, each of which can be classified into one of three major size classes: large (L1-L3), medium (M1=M3), and small (S1-S4). The L gene codes for three polypeptide chains, λA, λB, and λC; the M gene codes for polypeptide chains μA, μB, and μNS. The S genome contains three open reading frames (ơA, ơB, ơNS) that translate the fusion membrane proteins p10 and p17 and the membrane binding protein ơC, respectively. These viruses enter the host cell by receptor-mediated endocytosis (Bányai et al., Reference BÁNYAI, DANDÁR, DORSEY, MATÓ and PALYA2011).

In 1972, synovitis was described in hens. Serological tests revealed that synovitis was not related to Mycoplasma gallisepticum or M. synoviae. The agent that caused synovitis was determined to be similar to an agent of viral arthritis and identified as a reovirus. In birds, reovirus replication has been described in many tissues, but the target tissues of the virus are the intestines, tibio-tarsal joint and liver (Benavente and Martínez-Costas, Reference BENAVENTE and MARTÍNEZ-COSTAS2007).

A disease characterised by decreased body weight first appeared in broiler chickens in the late 1970s. The disease was described as ‘runting-stunting’ and was linked to several possible causative agents, including reoviruses (Jones, Reference JONES2008). Avian reovirus has been associated with RSS that is characterised by weight loss and has been subsequently associated with many possible causal agents. Several studies have described a vacuolar degeneration and detachment of the mucosa of the small intestine two days post-oral inoculation of the avian reovirus associated with enteric diseases in hens and chickens. Despite the replication in the intestinal epithelium and lesions in the small intestine, particularly lesions in the villi, this virus alone does not produce enteric disease; however, it does produce disease in combination with other enteric viruses (Songserm et al., Reference SONGSERM, ROOZELAAR, KANT, POL, PIJPERS and HUURNE2003).

Avian reovirus has been identified by RT-PCR in apparently healthy commercial chicken and turkey flocks, as well as in flocks presenting symptoms of enteric disease, principally diarrhoea (Pantin-Jackwood et al., Reference PANTIN-JACKWOOD, DAY, JACKWOOD and SPACKMAN2008; Jindal et al., Reference JINDAL, PATNAYAK, CHANDER, ZIEGLER and GOYAL2010).

Occurrence of enteric viruses in Brazil

Latin America is considered as one of the most important chicken producers, and Mexico and Brazil are the top producers. As in other countries, problems of enteric diseases have taken relevance in the poultry industry in this region. In Brazil, IBV (Villarreal et al., Reference VILLARREAL, BRANDÃO, CHACÓN, SAIDENBERG, ASSAYAG, JONES and FERREIRA2007), CAstV, avian nephritis virus, chicken parvovirus, FAdV group 1, avian reovírus, and avian rotavirus have been identified in chickens using PCR and RT-PCR (unpublished data). These viruses were detected in commercial birds which were presenting diarrhoea, lethargy, and ruffled feathers. The intestines of infected birds were filled with gas and undigested food. These symptoms are associated with enteric disease. Runting and stunting syndrome has also been reported, but its cause has not been fully determined. Many associations between enteric diseases and viruses, such as avian rotavirus, avian nephritis virus, chicken astrovirus, chicken parvovirus, infectious bronchitis virus, and fowl adenovirus, have been detected (unpublished data).

IBV has been detected in Argentina, Mexico, Chile, Colombia and Brazil. Many of these strains have been related to respiratory diseases (Cubillos et al., Reference CUBILLOS, ULLOA, CUBILLOS and COOK1991; Escorcia et al., Reference ESCORCIA, JACKWOOD, LUCIO, PETRONE, LÓPEZ, FEHERVARI and TÉLLEZ1997; Alvarado et al., Reference ALVARADO, VILLEGAS, MOSSOS and JACKWOOD2005; Rimondi et al., Reference RIMONDI, CRAIG, VAGNOZZI, KÖNIG, DELAMER and PEREDA2009), but in Brazil, the strains have been related to enteric problems (Villarreal et al., Reference VILLARREAL, BRANDÃO, CHACÓN, SAIDENBERG, ASSAYAG, JONES and FERREIRA2007).

FAdV group 1 has been detected in Brazil in the intestinal content of chickens with enteric problems, but it is undetermined if it was the cause of enteric diseases (unpublished date). Many reports from Peru, Ecuador, Mexico (Marek et al., Reference MAREK, GÜNES, SCHULZ and HESS2010), and Chile (Toro et al., Reference TORO, GONZALEZ, CERDA, HESS, REYES and GEISSEA2000) have associated the virus with IBH and HPS.

The others viruses mentioned in the present article, such as chicken parvovirus, chicken astrovirus, avian nephritis virus, avian rotavirus and avian reovirus, have been identified in Brazil in the intestinal content of chickens with enteric diseases (unpublished data). However, there are no reports of detection of these viruses from enteritis-affected cases in poultry in the rest of Latin America.