Avian rotavirus enteritis - an updated review.

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Avian rotavirus enteritis – an updated review a

a

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Kuldeep Dhama , Mani Saminathan , Kumaragurubaran Karthik , Ruchi Tiwari , d

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Muhammad Zubair Shabbir , Naveen Kumar , Yashpal Singh Malik & Raj Kumar Singh a

Division of Pathology, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India b

Division of Bacteriology and Mycology, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India c

Department of Veterinary Microbiology and Immunology, College of Veterinary Sciences, Pandit Deen Dayal Upadhayay Pashu Chikitsa Vigyan Vishwa Vidyalaya Evum Go-Anusandhan Sansthan (DUVASU), Mathura 281001, India d

Quality Operations Laboratory, University of Veterinary and Animal Sciences, Lahore 54600, Pakistan

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Division of Biological Standardization, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India f

Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India Accepted author version posted online: 28 Apr 2015.Published online: 18 May 2015.

To cite this article: Kuldeep Dhama, Mani Saminathan, Kumaragurubaran Karthik, Ruchi Tiwari, Muhammad Zubair Shabbir, Naveen Kumar, Yashpal Singh Malik & Raj Kumar Singh (2015): Avian rotavirus enteritis – an updated review, Veterinary Quarterly, DOI: 10.1080/01652176.2015.1046014 To link to this article: http://dx.doi.org/10.1080/01652176.2015.1046014

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Veterinary Quarterly, 2015 http://dx.doi.org/10.1080/01652176.2015.1046014

REVIEW ARTICLE Avian rotavirus enteritis a

an updated review

a

Kuldeep Dhama *, Mani Saminathan , Kumaragurubaran Karthik b, Ruchi Tiwaric, Muhammad Zubair Shabbird, Naveen Kumare, Yashpal Singh Malike and Raj Kumar Singhf a

Division of Pathology, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India; bDivision of Bacteriology and Mycology, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India; cDepartment of Veterinary Microbiology and Immunology, College of Veterinary Sciences, Pandit Deen Dayal Upadhayay Pashu Chikitsa Vigyan Vishwa Vidyalaya Evum GoAnusandhan Sansthan (DUVASU), Mathura 281001, India; dQuality Operations Laboratory, University of Veterinary and Animal Sciences, Lahore 54600, Pakistan; eDivision of Biological Standardization, Indian Veterinary Research Institute, Izatnagar, Bareilly 243122, India; fIndian Veterinary Research Institute, Izatnagar, Bareilly 243122, India

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(Received 9 February 2015; accepted 24 April 2015) Rotaviruses (RVs) are among the leading causes of enteritis and diarrhea in a number of mammalian and avian species, and impose colossal loss to livestock and poultry industry globally. Subsequent to detection of rotavirus in mammalian hosts in 1973, avian rotavirus (AvRV) was first reported in turkey poults in USA during 1977 and since then RVs of group A (RVA), D (RVD), F (RVF) and G (RVG) have been identified around the globe. Besides RVA, other AvRV groups (RVD, RVF and RVG) may also contribute to disease. However, their significance has yet to be unraveled. Under field conditions, co-infection of AvRVs occurs with other infectious agents such as astroviruses, enteroviruses, reoviruses, paramyxovirus, adenovirus, Salmonella, Escherichia coli, cryptosporidium and Eimeria species prospering severity of disease outcome. Birds surviving to RV disease predominantly succumb to secondary bacterial infections, mostly E. coli and Salmonella spp. Recent developments in molecular tools including state-of-the-art diagnostics and vaccine development have led to advances in our understanding towards AvRVs. Development of new generation vaccines using immunogenic antigens of AvRV has to be explored and given due importance. Till now, no effective vaccines are available. Although specific as well as sensitive approaches are available to identify and characterize AvRVs, there is still need to have point-of-care detection assays to review disease burden, contemplate new directions for adopting vaccination and follow improvements in public health measures. This review discusses AvRVs, their epidemiology, pathology and pathogenesis, immunity, recent trends in diagnostics, vaccines, therapeutics as well as appropriate prevention and control strategies. Keywords: avian; poultry; rotavirus; review; enteritis

1. Introduction Rotaviruses (RVs) are distributed across the world in humans and animals as the leading enteric pathogen. In poultry, a number of bacteria and viruses cause diarrhea either alone or in combination with other infectious agents (Andral et al. 1985; Saif et al. 1985; Reynolds et al. 1987; Saif et al. 1990; Perry et al. 1991; Hines et al. 1995; Jindal et al., 2010; Day & Zsak 2013; Koo et al. 2013). Among them, Escherichia coli, Salmonella and avian rotavirus (AvRV) are considered important pathogens (Estes & Cohen 1989; Tamehiro et al. 2003; Dhama et al. 2009). While examining the intestinal contents of turkey poults suffering from enteritis, AvRV was first identified in the USA in 1977 through electron microscopy (EM) (Bergeland et al. 1977) and later in the UK in 1978 (McNulty et al. 1978). Besides turkey poults, RVs have been isolated from other avian species that includes chicken, pigeons, pheasants, parrots, scoters and parakeets (Gough et al. 1985; Yason & Schat 1985; Saif et al. 1985; Gough et al. 1986; Takehara et al. 1991; Minamoto et al. 1988; McNulty 2003; Legrottaglie et al. 1997; Lublin et al. 2004; Dhama et al. 2009; Malik et al. 2013a). Although RV affects birds of all age groups, young birds (1 2

*Corresponding author. Email: [email protected] Ó 2015 Taylor & Francis

weeks) are most susceptible with high mortality (Dey 2003; Tamehiro et al. 2003; Islam et al. 2009; Yamamoto et al. 2011). In poultry, enteritis is a major clinical outcome of the disease that causes huge economic losses, because of decreased feed absorption and subsequent reduced weight gain, flock uniformity, and increased mortality (Guy 1998; Otto et al. 2006). Thus, AvRVs are considered as emerging pathogens with potential to cause huge economic losses to the growing poultry industry (Jones et al. 1979; Theil et al. 1986a; Holland 1990; Barrios et al. 1991; Dodet et al. 1997; Tamehiro et al. 2003; McNulty 2003; Jackwood et al. 2007; Chauhan et al. 2008; Dhama et al. 2009; Jindal et al. 2012; Malik et al. 2012, 2013a). As a consequence, control of rotaviral diarrhea is a major concern in poultry production sector which can be achieved by vaccination and sanitation. However, appearance of multiple groups in RVs and high genetic diversity within groups hinders production of an effective vaccine against AvRV (Borgan et al. 2003). Based on the antigenic sites located on the inner capsid of VP6 protein, RVs have been classified into eight groups (A H) (Estes & Cohen 1989; Estes & Kapikian 2007; Marthaler et al. 2014). In poultry, these are


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clustered to groups A, D, F and G (Otto et al. 2006; Trojnar et al. 2010; Johne et al. 2011). The RVA are mainly associated with diarrhea in humans, various domesticated and captive mammals, and poultry (Matthijnssens et al. 2008; Matthijnssens & Van Ranst 2012). They have been frequently isolated from young birds placed in commercial turkey or chicken rearing units with varying ages. Turkey poults, for example, have been often infected during their first week of life while broiler chickens were generally found infected at about four weeks of age (Theil & Saif 1987). RVD, RVF and RVG have been seen exclusively in poultry (Urasawa et al. 1992; Saif & Jiang 1994; Santos & Hoshino 2005; Kattoor et al. 2013a; Kattoor et al. 2013b) and may contribute to disease (McNulty et al. 1984; McNulty 2003; Villarreal et al. 2006). The D group has also been frequently detected in avian species. However, a few molecular studies are available revealing its genetic information. They were first identified in late 1990s (Pedley et al. 1986; Theil et al. 1986b) followed by subsequent reports from Europe (Lojki et al. 2009; Johne et al. 2011) and Asia (Ahmed & Ahmed 2006; Otto et al. 2012). AvRVs of groups F and G have been identified occasionally (Bezerra et al. 2012; Otto et al. 2012). Recently, similar to condition caused by avian reoviruses, it has been suggested that RVs may also cause runting and stunting syndrome in poultry (Otto et al. 2006). In recent years, co-infections of AvRV in addition to other enteric pathogens such as astroviruses (AsTVs) and coronaviruses (CoVs) have been recognized to cause enteritis in poultry flocks (Chandra et al. 2001). Poult enteritis syndrome (PES) has been reported by Minnesota turkey growers and poultry veterinarians (Jindal et al. 2009, 2010). In India, the presence of AvRVs belonging to group A has been reported from limited geographical areas originating from northern and central parts of the country. Thus, very little is known about the circulation of AvRVs in Indian poultry flocks (Savita et al. 2008a; Malik et al. 2013a). The present review discusses the AvRVs, their epidemiology, pathology and pathogenesis, immunity, and recent trends in diagnosis, vaccines, therapeutics as well as appropriate prevention and control strategies. 2. Virus, classification and genome organization Intact RV virion consists of two icosahedral capsid shells of approximately 50 and 70 nm in diameter. A distinctive ‘wheel-like’ appearance, as seen through negative-stain EM, results from smooth outer rim and capsomeres of inner capsid that radiate towards rim (Guy 1998). Genome consists of 11 double-stranded (ds) RNA segments (Figure 1) protected by a triple-layered wall, out of which two layers are contributed by icosahedral capsid protein (Guy 1998; McNulty 2003). The ds RNA have a molecular weight of approximately 12£ 106 Da, and each RNA segment consists of open reading frame (ORF) that encodes viral proteins (Estes & Cohen 1989; Guy 1998). Viral genome encodes six structural and non-structural proteins each (Mori et al. 2002a), out of which 10 major

polypeptides have been identified for their prominent roles (McNulty 2003). The protein VP2 forms the first layer, encompassing proteins VP1 and VP3, both of these together have a role in virus transcription. The VP6 protein (encoded by 6th gene segment) forms the second layer and the outermost protein layer is composed of structural proteins VP7 (encoded by 7/8/9th gene segment based on the strain) and spike protein VP4 (encoded by 4th gene segment). VP7 (denoted as ‘G’-glycoprotein) and VP4 (denoted as ‘P’-protease sensitive protein) proteins are capable of generating neutralizing antibodies that protect birds from disease (Niture et al. 2010b). Also, VP4 can undergo proteolytic cleavage that further enhances infectivity of RVs (McNulty 2003) (Figure 1). Among non-structural proteins (NSP), NSP4- a viral enterotoxin, is known to have major differences in amino acids when compared to similar protein in mammalian RVs (Mori et al. 2002a; Kusumakar et al. 2010). Replication and assembly of RVs occurs in the cytoplasm of host cells and virus particles are commonly found within vacuoles. RVs are relatively heat-stable and their infectivity is not affected by ether and low pH (Guy 1998). The AvRV is classified under the genus Rotavirus within the Reoviridae family. Among RVs, there are eight major groups (A to H) identified with RVA being the most predominant across the world (Yang et al. 2004; Matthijnssens et al. 2011). Classification of AvRVs was initially ascertained by cross-immunofluorescence studies or polyacrylamide gel electrophoresis (PAGE) analysis of ds RNA segments (Guy 1998). AvRVs that cross-react with antisera prepared against group A mammalian RVs are classified as RVA. The RVs which lack RVA antigen are referred to as atypical RVs that belong to groups D, F and G (Guy 1998; McNulty 2003; Otto et al. 2012; Hemida 2013). The AvRVs are antigenically related and morphologically identical to mammalian RVs (McNulty et al. 1978, 1979). The genomic RNA segments cluster into four regions I to IV. The AvRVA has a pattern of 5:1:3:2, RVD has a pattern of 5:2:2:2, while mammalian RVA show a pattern of 4:2:3:2, respectively (McNulty et al. 1981). Typical electropherogram for uncommon RV groups, known as F and G (4:1:2:2 and 4:2:2:3, respectively) that are quite different from group A, B, C and D, was first described by McNulty et al. (1984) in gut contents of chickens from Northern Ireland. Since then, both RVF and RVG have been detected in feces of turkeys (Kang et al. 1986; Theil et al. 1986b; Otto et al. 2012) and broiler chicks (Otto et al. 2006, 2012). Sequencing of VP6 genes of these avian RVF and RVG groups shed light on their possible evolution process (Johne et al. 2011). RVF was found most closely related to AvRVA and RVD (49.9% 52.3% nucleotide and 36.5% 39.0% amino acid sequence identity), while group RVG was found most closely related to mammalian group B (55.3% 57.5% nucleotide and 48.2% 49% 9% amino acid sequence identity). Recently, full genome of both groups (F strain 03V0568 and G strain 03V0567) has been deciphered and revealed low nucleotide sequence identities with other RVs that ranged between 29.8% (NSP1 gene) and 61.7%


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Figure 1. A schematic overview of rotavirus structure. Virus showing icosahedron symmetry with capsid containing 11 genome segments (dsRNA) of varying lengths. Various structural and nonstructural proteins are coded by the monocistronic genome segments.

(VP1 gene) for RVF, and between 29.3% (NSP1-2 gene) and 65.9% (NSP2 gene) for RVG (Kindler et al. 2013). Phylogenetic analysis placed RVs in two major clades consisting of rotavirus A/C/D/F and rotavirus B/G/H (Kindler et al. 2013). Within these clades, with similar findings as described earlier (Johne et al. 2011), RVF mainly clustered with RVD while RVG clustered with RVB. Emergence of these uncommon groups highlights high diversity of RVs as a result of a complex evolutionary history. We earlier studied the evolution of codon usage patterns in virus host system in AvRV of groups RVA, RVD, RVF and RVG which are preferentially affecting birds employing multivariate statistical methods targeting over expressive VP6 protein constituting inner capsid of the virion. The results confirmed the bias in codon usage in AvRVs with distinctive preference for certain codons. The opinion that few of the codons which are rare in chicken cells (TTA for Leu, TCG for Ser and CCG for Pro) are not uncommon in AvRVs, points towards the evolution of virus with its preferred host. More precisely, the comparative analysis results of AvRV and relative synonymous codon usage (RSCU) values indicate that the codon usage pattern of AvRV is coinciding with that of its chicken host. Comparative analysis results, in which specific clustering of isolates based on country of origin was observed, also noted paving a new light to the evolutionary pattern of the RV affecting poultry species. The findings highlight genetic diversity and codon usage in AvRVs and provide a step forward to recognize the procedures impelling the evolution of avian viruses (personal unpublished data). Currently, classification of RVA is done on the basis of molecular properties of VP4, VP6 and VP7 proteins. As re-assortment of all 11 segments of the gene of RVs play a key role in generation of diversity of RVs in nature, it is required to have a classification

system on the basis of all gene segments of RVs. On the basis of phylogenetic analysis, appropriate determination of identity cut off values has been assessed for each gene. A nucleotide identity cut off value of 80% has been established for VP4 gene, whereas for VP7 gene, identification of four additional genotypes including AvRV strains have been identified (Nicholas et al. 1997; Matthijnssens et al. 2008). The first complete genome sequence of RVDs was assessed using sequence-independent amplification strategies and degenerate primers (Trojnar et al. 2010). ORFs that encode homologues of proteins of RVs (VP1 to VP4; VP6 and VP7; NSP1 and NSP5) have been identified. Between RVDs and RVs belonging to groups A, B and C, amino acid sequence identities have been found to vary (Trojnar et al. 2010). Common evolution of group A, C and D has been particularly determined by phylogenetic analysis (Trojnar et al. 2010; Kindler et al. 2013). It is interesting to note that sequences of nucleotide at termini of 11 genome segments have been found to be identical between RVD as well as RVA (Trojnar et al. 2010). In case of mammalian RVA, segment 5 was found to migrate closer to 6, whereas in AvRVs, segments 7, 8 and 9 were found to migrate as a tight triplet (Wani et al. 2003). The physicochemical properties of AvRVs have also been studied. It has been found that they are endowed with tremendous stability and resistance. RVs have a buoyant density of 1.36 g/cm3 and are stable at pH 3.0, relatively heat tolerant and resistant to ether, chloroform, quaternary ammonium compounds and chlorination procedures (McNulty 2003). However, they are sensitive to phenol and formaldehyde (Takase et al. 1986; Kang et al. 1988; Minamoto et al. 1988; Minamoto & Yuki 1988). The AvRV can also survive in poultry manure for long periods. In general, several factors are responsible for the time needed for reduction of 90% rotavirus titer, including

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ambient temperature, pH, and type of waste, the RVs survive to nearly 60 days (Guy 1998; Boone and Gerba, 2007) to up to 6 months in environment (Sobsey & Meschke 2003). 3. Epidemiology Virus associated gastrointestinal diseases have a tendency to preponderate mainly young chicks. Other infectious agents convolute these diseases under field conditions, for example, AsTVs, enteroviruses, reoviruses, paramyxovirus, Salmonella, E. coli, and cryptosporidium (Reynolds et al. 1987; Gough et al. 1990; Saif et al. 1990; Perry et al. 1991). It becomes problematic as far as measurement of agents’ factual role in natural befalling gastrointestinal disease is concerned. Therefore, it is of utmost importance to understand epidemiology of AvRVs for developing appropriate control measures (Pedley et al. 1986; Estes & Kapikan 2007). In poultry, both layer hens and broilers, RV has already been established as an agent that causes enteritis and diarrhea. Symptoms occur due to prolific viral replication in intestinal epithelium, resulting in nutrient mal-absorption; finally affecting feed conversion ratio and inflicting severe economic losses to poultry industry (McNulty 2003; Villarreal et al. 2006). Although RV disease in broiler chicken occurs mostly in winter season (Alam et al. 1994), the disease has been recorded mainly in summer season in south-eastern region of Asia (Ahmed & Ahmed 2006; Karim et al. 2007). Many reports have shown that flocks of broilers and turkeys frequently experience simultaneous/sequential diseases with different RV groups (McNulty et al. 1984; Todd & McNulty 1986; Reynolds et al. 1987; Theil & Saif 1987) and mixed disease with other enteric pathogens (Andral et al. 1985; Saif et al. 1985; Reynolds et al. 1987; Gough et al. 1990; Perry et al. 1991; Hines et al. 1995; Yu et al. 2000). Presence of virus in fecal material and extreme resistance of viruses have paved way for a persistent presence of this disease in poultry environments. Water as well as sewage and inanimate objects have been found to be rich sources of RVs detected in poultry sheds (Brussow et al. 1992a; Rohwedder et al. 1995, 1997; Mori et al. 2001; Savita et al. 2008a). The RV enteritis in poults and chickens has been reported from UK, USA, France, Argentina, Brazil, China and Russia (McNulty 2003). In the south-eastern part of Asia, the prevalence of RVs in avian species varied from 2.9% to 22.5%. Highest prevalence has been observed (40%) in 12-day-old birds while the lowest was observed in birds aging 22 days (6%) (Ahmed & Ahmed 2006; Karim et al. 2007). A recent study in Brazil revealed 53.8% prevalence of rotavirus from broilers, layers and broiler breeders (Beserra et al. 2014). In countries like Bangladesh, RV disease is reported as 0.9% of diarrheic broilers (Ahmed 2013). In central part of India, group D RVs have been reported to be more prevalent (77.8%) than RVA (22.2%) along with presence of strains that are genetically diverse in nature (Savita et al. 2008a). The disease incidence in such major poultry producers indicates significant distribution that could become a potential threat and a grave

problem in near future. The major obstacle in controlling disease is attributed to high antigenic variation particularly due to antigenic shift (Iturriza-Gomara et al. 2004; Simmonds et al. 2008). Kattoor et al. (2013a) conducted an epidemiological study to discern existing status of avian RVA and RVD prevailing in different states of India. Out of 215 diarrheic fecal samples collected from chickens of 1 8-weeks-old, 7 (3.3%) were positive in polyacrylamide gel electrophoresis and silver staining (PAGE-ss), while 25 (11.6%) were positive in RT PCR for RVA. Only 3 cases were positive for both RVA and RVD in RT PCR. In RNA PAGE, RV positive samples showed typical mammalian group A specific genomic pattern (4:2:3:2). The regional distribution of AvRVs revealed high prevalence in Uttarakhand (7.4%) followed by Haryana (2.8%) and Kerala (1.3%). None of the samples from Uttar Pradesh and Tamil Nadu was found positive for AvRV. Although RV causes diarrhea in different species like human infants, calves, lambs, goat kids, piglets and puppies in different parts of the world (Georges et al. 1984, Garcia et al. 2000, Wani et al. 2004; Dhama et al. 2009), reports regarding circulation of AvRVs are scarce in India. Wani et al. (2003) first detected the mammalianlike electropherogroup AvRVs from chicken with diarrhea. Minakshi et al. (2004) detected the AvRVA from diarrheic feces of poultry. Savita et al. (2008a) reported higher incidence of RV detection from diarrheic samples (17.4%) than environmental samples (3.2%). From samples obtained from 7 different farms with history of diarrhea, Savita et al. (2008b) reported that 11.7% had mixed etiology for diarrhea comprising of 6.5% as E. coli and AvRV diseases. Both atypical mammalian group and typical avian group RVA have been detected in India (Wani et al. 2003; Minakshi et al. 2004; Savita et al. 2008b). Niture et al. (2010a) reported that 7.84% of poultry were positive for RVD in Maharashtra and electropherotyping revealed 5:2:2:2 migration patterns. Kattoor et al. (2013b) reported for the first time sequence-confirmed RVD disease in 1 to 2 week old broiler chicks from Tarai area of the temperate western Himalayan region in northern India. 4. Host range AvRVs naturally infects and replicates well in turkeys, chickens, pheasants, partridges, ducks, guinea fowl, pigeons, scoters and lovebirds, where some of these have been experimentally infected (McNulty et al. 1980; Minamoto et al. 1988; Takehara et al. 1991; Legrottaglie et al. 1997; Otto et al. 2006; Pantin-Jackwood et al. 2007). Most of natural AvRV diseases occur during age of less than 6 weeks in turkeys, chickens, pheasants, partridges and ducks. Paradoxically, chickens and turkeys were more susceptible to experimental disease with RV in older ages (56 to 119 days) than birds in first few weeks of life (Yason & Schat 1986b, 1987). However, in field situation, evidence indicates that most of turkeys and chickens will have been infected, and presumably will have developed some immunity, well before this age (Myers & Schat 1990a, 1990b). Added to this, Jones et al. (1979) reported


Veterinary Quarterly lack of age resistance to disease as well as an outbreak of rotaviral diarrhea that occurred between 32 and 92 weeks of age in commercial laying hens. In wild avian species like pheasants (Phasianus colchicus) very low prevalence of RVA (0.3%) has been reported (Ursu et al. 2011). It has been suggested previously that RVs of avian species are separated from RVs of mammals early during the process of evolution. They have got more similarity to RVs of avian species than to RVs of mammals in terms of both genetic as well as antigenic properties. Brussow et al. (1992a, 1992b) isolated avian-like RVA from a calf with clinical signs of diarrhea in Germany based on RNARNA hybridization, nucleotide sequencing and antigenic examination. Sequence analysis of VP6, VP7 and VP8 from RV 993/83 showed high similarity with the Japanese pigeon RV PO-13 (Rohwedder et al. 1995). These results clearly indicate that RV993/83 is an AvRV that had been transmitted to calves. However, there is no direct evidence that AvRV cause enteritis in calves or other mammalian species. Nevertheless, Mori et al. (2001) demonstrated the first evidence of AvRV being experimentally transmissible to a mammal by oral inoculation with two AvRVs such as pigeon rotavirus (PO-13) and turkey rotavirus (Ty-3) in suckling mice. The pigeon RV did infect and induced diarrhea, but turkey RV did not induce diarrhea in suckling mice. Besides, there are also reports of mammalian RVs having the ability to get transmitted to avian species (Wani et al. 2003; Schumann et al. 2009). 5. Mixed infections Multiple enteric infections are a serious threat with fatal outcome compared to infection by one causative agent. Initial identification of those multiple infections is essential for formulating the better treatment recipes and preventive measures on the long term. Andral et al. (1985) and Saif et al. (1985) first reported mixed disease with RV, reovirus, adenovirus and pseudo-picornavirus in chicken and turkey poults with clinical history of diarrhea. From intestinal samples of turkey poults (between 1 day and 5 weeks of age), Reynolds et al. (1987) revealed AsTVs (78%) as the most prevalent co-infection followed by rotavirus-like viruses (RVLVs) (67%), RVs (22%), atypical RVs (12%), enteroviruses (5%), and reoviruses (2%). With clinical signs of scour and stunting, Gough et al. (1990) reported RV (13.9%), adenovirus (0.9%), reovirus (0.9%) and enterovirus (0.9%) from game birds such as pheasants, partridges and quail. Saif et al. (1990) isolated RVD, Salmonella, AsTV and a small round virus (18-24 nm in diameter) from natural outbreak of enteritis in turkey poults. Perry et al. (1991) reported mixed disease of cryptosporidium, RV, paramyxovirus and Salmonella from naturally occurring cases of poult enteritis with skeletal lesions. Hines et al. (1995) reported mixed disease of adenovirus, RV and E. coli from Emu chicks with a history of hemorrhagic enteritis. Yu et al. (2000) reported turkey coronavirus (TCoV), AvRV and reovirus from intestinal samples of turkey poults affected with PEMS. In addition to other enteric pathogens of bacteria (E. coli, Enterococcus), viruses (enterovirus, reovirus and

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adenovirus) and protozoa (Eimeria spp), PEMS has frequently been associated with higher proportion of AvRV (93%), turkey astrovirus-2 (84%) and Salmonella by RTPCR (Jindal et al. 2009, 2010). Koo et al. (2013) reported an unusual case of concomitant disease with 23.8% of chicken AsTV and 14.3% of RVA in broilers with a history of enteritis. Recently, Roussan et al. (2012) reported mixed disease of RV along with AsTV, reovirus and adenovirus group I in broiler flocks of Jordan. 6. Transmission The RVs of avian species especially pigeon RVs play a crucial role as a pathogen that can cross species barrier to infect mammals (suckling mice) and induce diarrhea (Mori et al. 2001, 2002a; Villareal et al. 2006), but evidence for vice-versa is lacking (Saif & Jiang 1994). Several investigators have reported natural cases in which inter-species transmission of AvRVs (RV 993/83), especially to bovines as well as experimental animals has been reported (Brussow et al. 1992a, 1992b; Mori et al. 2001, 2002a; Tamehiro et al. 2003; Ahmed & Ahmed 2006). Besides, there are also reports of mammalian RVs having the ability to get transmitted to avian species (Wani et al. 2003; Schumann et al. 2009). The resistance and the extreme stability permit the persistence of the virus in the environment, a key factor in transmission of disease to susceptible birds (Brussow et al. 1992a; Rohwedder et al. 1995, 1997; Mori et al. 2001). The RVs can survive in waste for 2 to 6 months (Guy 1998; Boone and Gerba, 2007). Huge quantum of ARVs is excreted via avian feces and horizontal transmission readily occurs by oral route or direct contact (McNulty 2003). Rotavirus prevalence has been reported to be relatively high in turkey manures (Lublin et al. 2004). There are no reports of vertical or egg transmission of RVs in flocks till to date. Theil and Saif (1987) detected RVs in 3-day-old turkey poults that provoked the assumption that transmission occurs either in or on egg. No evidence is available for a carrier state of RVs in birds. Despins and Axtell, 1994 demonstrated darkling beetle larvae as a mechanical vector for turkey RVs. 7. Clinical signs Variations in virulence and severity of clinical signs associated with different rotavirus strains have been reported. The pathogenesis and clinical signs of group A rotavirus in birds has been well established (Pantin-Jackwood et al. 2008; Schuman et al. 2009; Trojnar et al. 2009; Jindal et al., 2010; Ursu et al. 2011). Prevalence of groups D, F and G RVs has only been described recently (Trojnar et al. 2010; Johne et al. 2011; Otto et al. 2012) and yet, studies on pathogenesis and clinical signs in birds are lacking. Haynes et al. (1994) reported high mortality rate in pheasant chicks associated with group D rotavirus. Otto et al. (2012) reported that group A and D rotavirus were dominated in chickens and turkeys causing diarrhea, growth retardation and/or runting and stunting syndrome (RSS). Several studies clearly show that AvRV-D was the most commonly found rotavirus in turkeys (McNulty and


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Reynolds 2008; Reynolds et al. 1987; Theil et al. 1986c). Some studies demonstrate broiler chickens of 7 12 days of age as highly susceptible to RVD as compared to other age groups (Karim et al. 2007; Islam et al. 2009). Furthermore, Bezerra et al. (2014) reported occurrence of group D rotavirus in apparently healthy asymptomatic chickens. Rotavirus disease of avian species can vary from subclinical to severe enteritis. Apart from dehydration and anorexia, weight loss as well as increased mortality are characteristic features (McNulty 1997; McNulty 2003; Tamehiro et al. 2003). Diarrhea is the principal manifestation of disease, while in affected birds, decreased weight gain, dehydration and an increased mortality could also be observed (McNulty 2003). In young chickens, milder version of disease may be noticed that can lead to a more severe clinical manifestation in chickens of age group between 12-21 days. This is mainly characterized by unrest and ingestion of litter, watery feces, wet litter, and severe diarrhea (Barnes 1997). There are also reports of mixed disease caused by E. coli and Salmonella along with RVs (Savita et al. 2008b). However, variation in severity of RV diseases has been noticed. This might be due to the differences in virulence of RV strains or interaction of other infectious agents, environmental stress or management factors (McNulty 1997). Turkey poults have been found to be more susceptible than chickens (Yason et al. 1987; Yason & Schat 1987). Severity of symptoms has been seen more frequent in 12 to 21-day-old chickens showing unrest, ingestion of litter, watery feces or diarrhea (McNulty 2003). In field conditions, besides enteritis and diarrhea, RV diseases may be associated with anorexia (McNulty 2003; Tamehiro et al. 2003). In broilers mal-absorption may also be seen (Lublin et al. 2004). Besides, immunosuppression and outbreaks of other intestinal pathogens like Clostridium or coccidia is common during RV disease (Lublin et al. 2004). Similarly, in pet birds like pigeons or parakeets, RVs are one of the causes of gut dilatation and impaired food absorption. Watery diarrhea has been a common finding in infected pigeons. Compared to pigeons, AvRVs are less commonly seen in pet birds like parrots and parakeets. The manifestations observed in such pet birds include diarrhea and proventricular dilatation due to the presence of undigested food (Lublin et al. 2004). In general, experimental inoculation of chickens and turkeys with avian RVs results in mild to inapparent disease. Mixed disease due to both chicken AvRV as well as astrovirus (CAstV) has been reported by Koo et al. (2013). Such kind of mixed disease has been more intensely identified in broiler flocks. Significant lesions in the intestine have been identified in birds belonging to this group where characteristic features includes frothy contents and paleness along with thin walls of intestine. Otto et al. (2006) reported that group D rotavirus plays a major role in pathogenesis of runting and stunting syndrome (RSS) in flocks with severe villous atrophy. Jindal et al. (2009) also reported RSS of unusual nature in chicken with high mortality and retarded growth.

8. Pathogenesis The RVs present in environment gains entry into body through ingestion, after which replication commences, mainly in mature villus epithelium of small intestine (McNulty 1997, 2003). The outer capsid protein VP4 plays an important role in initiating a viral infection via attachment and entry. The VP4 gets cleaved into two fragments known as VP5 and VP8. The VP8, the globular head of the spike, interacts with host receptor resulting in attachment and entry of virions into host cells. Sugiyama et al. (2004) demonstrated that cell attachment protein (viral protein 8- VP8) utilize sialic acid containing molecules as receptors on surface of MA104 cells in vitro but confirmation of similar mechanism in in vivo models are lacking. The dual capsid protein coat makes virus very resistant to stomach pH and digestive enzymes in the gastrointestinal tract (Figure 2). Infectivity of virus is enhanced by proteolytic cleavage of viral protein VP4 (spike). Specifically, RV invades epithelial cells especially at the edges of intestinal villi, and subsequent viral replication results in lysis of host intestinal cells, thereby impairing nutrient absorption. AvRVs causes decreased glucose-stimulated sodium transport and net absorption of sodium, potassium, chloride and water resulting in rapid onset of severe, watery diarrhea with loss of electrolytes in feces (Hamilton & Gall 1982). After efficient multiplication of AvRV, progeny virions are excreted via feces within a period of 2 to 5 days post exposure (McNulty et al. 1983; Guy 1998). In birds, besides small intestine, viral multiplication has also been observed in colon and cecum (Lublin et al. 2004). Diarrhea, a significant manifestation, occurs due to destruction of mature villous enterocytes and replacement by immature epithelial cells from crypts (Moon 1978). The immature crypt cells replace destroyed mature enterocytes that lack disaccharidases and have impaired absorptive ability, resulting in diarrhea (Moon 1978; Guy 1998; McNulty 2003). Yason & Schat (1986a) reported frothy fluids present in ceca of infected birds that caused impaired digestion as well as absorption of carbohydrates and sugars, resulting in fermentation by caecal bacteria, producing metabolites that absorb water into ceca by osmosis. Similarly, diarrhea may also occur as a result of mal-absorption and mal-digestion. However, recently one of non-structural proteins, NSP4, has been attributed to a major cause of rotavirus-mediated disease pathogenesis. NSP4 has been shown to be an enterotoxin that is capable of causing diarrhea (Figure 2). When this protein is expressed and released in the lumen of the intestine, it interacts with adjacent enterocytes, activates a signal transduction pathway resulting in enhanced chloride secretion through a calcium-dependent pathway by mobilizing calcium from the endoplasmic reticulum, thus causing secretory diarrhea (Ball et al. 1996; Kapikian et al. 2001; Mori et al. 2002a, 2002b). Also, it has been reported that mutation in NSP4 may act as a factor for variation in virulence of AvRV isolates (Zhang et al. 1998). In host, for countering viral pathogenesis, intra-epithelial



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Figure 2. Avian rotavirus replication and pathogenesis. Virus enters the small intestinal cells through the sialic acid receptor. Triplelayered viral particle enters cell through endosome. Endosomal membrane is ruptured by VP4 and VP7. Double-layered viral particle is formed by shedding of VP7. Viroplasm is the area where viral proteins and structures are assembled. Damage to villi leads to release of virus and this also causes diarrhea. NSP4 acts as enterotoxin and it also has various roles in pathogenesis.

lymphocytes (IEL) may have a key role to play together with a prompt natural killer (NK) cell activity (Myers & Schat 1990a). When compared to bovine and porcine RVs, there exist ample differences in pathogenesis and lesions caused by AvRVs. Shortening of villi in experimentally infected turkeys (Yason et al. 1987; Hayhow & Saif 1993; Shawky et al. 1993) and chickens (Yason et al. 1987) were less severe when compared to RV infected calves and piglets. These differences may be due to differences in development of intestinal villi between infected mammals and birds (Yason & Schat 1986a, 1987; Yason et al. 1987). Mammalian RVs replicates in macrophages in blood vessels and lungs, and cause histopathological changes in cells of liver and lungs. However, it is not known if a similar situation occurs in RV infected birds. The replicative mechanism of RVs within host cells has also been ascertained (Desselberger et al. 2005). The AvRV gets entry into intestinal epithelial cells via endocytosis and is encapsulated in a vesicle called endosome. Then, proteins in the outer layer (VP4 and VP7) disrupt the endosomal membrane by creating an imbalance in calcium ion concentration, after which breakdown of VP7

trimmers into single protein subunits occur, leaving VP2 and VP6 coats around viral ds RNA to form a double layered particle (DLP). After this, virus generates viral mRNAs with help of RNA-dependent RNA polymerase. So, as disease progresses, RVs produce mRNAs to facilitate both protein translation and replication of viral genome. Later on, most of RV proteins get accumulated in structures known as viroplasms, where replication occurs and DLPs are assembled. Non-structural viral proteins, NSP5 and NSP2, form such viroplasms or viral factories (Figure 2). The DLPs then migrate to endoplasmic reticulum to obtain outer layer (VP4 and VP7), and thereby finally develop into a complete ‘double capsid and triple-layered’ infectious virus particle (Attoui et al. 2012). Yason and Schat (1986a) had examined the pathogenesis of disease due to RV by infecting conventional and specific-pathogen-free (SPF) eggs of turkey poults of 7 to 10-days and 42-days-old. They observed remarkable infiltration of leukocytes in the lamina propria, and epithelial cell vacuolation along with villous surface scalloping at the tips. Moreover, at 2-4 days post infection there has been significant impairment in the level of D-xylose

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absorption in the intestinal tract (Yason & Schat 1987; Hayhow & Saif 1993; Shawky et al. 1993). 9. Gross lesions and histopathology The major pathological lesions of RV enteritis in birds include whitish-transparent intestinal walls, enlarged gall bladder, and atrophy of the pancreas along with degeneration of bursa of Fabricius, rickets and proventriculitis (Lublin et al. 2004). Large amount of fluids and gas could be seen in intestine and ceca. The carcass may be dehydrated, reveal stunting growth, pasted and inflamed vents, anemia due to vent pecking, litter in gizzard and inflammation of plantar surface of foot (Bergeland et al. 1977; Horrox 1980; McNulty et al. 1980, 1983; Yason et al. 1987; Hayhow & Saif 1993; Shawky et al. 1993; Haynes et al. 1994). In some cases, hemorrhages are also noticed in caecal walls especially in pheasant chicks (Gough et al. 1986). Discrete, multifocal, superficial brownish red erosions may be present, primarily in duodenum and jejunum of experimentally infected turkeys at 84 to 112 days of age (Yason et al. 1987; McNulty, 2003). Histopathology shows vacuolation of enterocytes, separation and desquamation of enterocytes from lamina propria, and infiltration of inflammatory cells in lamina propria (McNulty 2003). Mature villous absorptive epithelial cells in distal third of small intestine are mostly affected. Also, there could be infiltration of inflammatory cells in cecum. In affected birds, with loss of microvilli, length of villi in duodenum and jejunum may be considerably shortened. Degeneration, inflammation and atrophy of villi can also be found in jejunum in some instances (Ciarlet et al. 1998). Enough damage may perhaps be caused due to RV disease that allows exposure of lamina propria to certain chemotactic agents from both poly-morphonuclear as well as mononuclear cells. However, it is important to note that, in pigs as well as calves, RV can cause damage to a larger villus area (Yason & Schat 2013). Within RV, different groups may show preference for specific areas in small intestine for replication. RVA grows best in duodenum of experimentally infected chickens, whereas RVD grows best in jejunum and ileum (McNulty et al. 1983). Generally, in RV infected birds, decrease in mean villous lengths as well as increase in crypt depths results in reduced villus to crypt ratios. Subsequent to this, morphometric changes are more pronounced in duodenum and jejunum than ileum (Hayhow & Saif 1993; Shawky et al. 1993; Yason et al. 1987). While conducting histopathology, a pigeon RV (PO-13) has been detected sporadically in ileal absorptive cells. Lesions such as ballooning and degeneration of cells are observed in the region from duodenum to ileum (Mori et al. 2001, 2002a). Although no significant histopathological changes are generally seen in naturally acquired RV disease in poults (Horrox 1980), degeneration and inflammation of villi of duodenum and jejunum has been reported in poults with experimental rotaviral enteritis (Bergeland et al. 1977). Lesions have not been found in ileum, cecum, colon, cloaca, or other organs. Neither gross nor microscopic lesions are pathognomonic for RV disease.

10. Immunity to avian rotaviruses 10.1. Passive immunity Maternally derived antibodies against RV are passively transferred to the avian embryo through egg yolk (Figure 3). This antibody titer progressively decreases in serum and is undetectable at 3 4 weeks of age (Yason & Schat 1986a). Presence of maternal antibodies in serum does not influence or prevent susceptibility of chickens and turkeys to experimental RVA disease (Meulemans et al. 1985; Yason & Schat 1986a). However, poults of hyper-immunized turkey hens harboring circulating maternal antibodies (IgG) were more resistant to experimental RV disease at the age of 2 to 5 days than at 12 days (Figure 3). It was emphasized that circulating maternally derived IgG protects the intestinal mucosa during first week of life against RV disease (Meulemans et al. 1985; Yason & Schat 1986a; Shawky et al. 1993). Turkey poults hatched from hyper-immunized or vaccinated turkey hens carry maternally derived anti-rotavirus IgG (rIgG) antibodies. During the first week of life, antibody titer in turkey poults was 200 500 times less in intestinal washings than in serum and it was further negligible at 10 and 13 days of age in intestinal washings. Evidence showed that rIgG gets transferred from blood to the intestine. However, maternally derived rIgG could not be detected in intestinal washings of poults hatched from naturally infected hens (Shawky et al. 1994). The role of IgA on passive immune response of birds to rotavirus infection has not been studied yet.

10.2.

Active immunity

Older birds generally develop higher antibody titers and respond more quickly than younger birds. Oral inoculation of chicken and turkeys showed serum antibody responses as early as 4 6 days post disease (Yason & Schat 1986a, 1986b, 1987). Information regarding development and duration of immunity to RVs following disease of birds are scarce. Myers et al. (1989) reported kinetics of antibody responses in chickens experimentally inoculated with RVA. Rotavirus specific IgM, IgG and IgA were detected in serum where intestinal antibody response entirely consisted of IgA (Figure 3). Myers and Schat (1990a), as an important in vivo immune response, demonstrated NK cell activity in chick intra-epithelial leukocytes against RVs. Myers and Schat (1990b) further reported that intestinal antibodies (IgA) alone are not only a mediator for recovering from disease, but also must regarded as development of resistance to re-disease. An increase in serum neutralizing antibodies was observed in pheasant hens vaccinated through intramuscular route with an inactivated group A pheasant RV vaccine. Hens at 1 2 days of age were challenged with RVA and mortality in progeny of vaccinated hens was significantly less (19.4%) as compared to controls (48.3%) (Gough et al. 1999). These results suggest that maternally derived antibodies in progeny of unvaccinated turkeys and pheasants are not providing significant protection against a field challenge with RV. A much higher titer of



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Figure 3. Immunity to avian rotavirus. Active immunity- oral administration/infection of birds with avian rotavirus leads to antibody development (IgA-intestine; IgM, IgG-serum). Passive immunity-transmission of antibodies from immunized bird to egg/chick. Maternal antibodies protect chicks against infection.

antibody would be needed to completely protect young birds during their first week of life.

11. Diagnosis Earlier, RV in poultry flocks have been diagnosed though EM. Although it is a sensitive diagnostic approach that detects RVs of all serogroups (Theil et al. 1986c), it is a costlier and cumbersome option. Compared to this, PAGE is equally sensitive as well as highly efficient in AvRV grouping (Guy 1998) that is being used for demonstration of genomic segments of RV- RNA (Theil et al. 1986c; Theil 1987), its epidemiology and classification. For rapid diagnosis of RV disease, direct detection of 11 different segments of RNA and their typical pattern of migration in PAGE has been performed via silver staining (Svensson et al. 1986). While comparing electrophoretic migration patterns of human as well as avian RVs, a distinct migration pattern of AvRVs was found compared to electropherotypes in human strains (Villareal et al. 2006). Savita et al. (2008a) reported two different electropherotypes within group A avian RVs. This indicates existence and circulation of genetically diverse strains of avian RVs. When compared with other types, migration pattern of RNA segments of avian RVAs showed short

electropherotypes (migration of the 10th and 11th segment occurs closely). However, differences lie in other segments. Segments 4 and 5 migrated closely in environmental rotavirus positive sample, while they were distant in another group A rotavirus sample. Genome segments 7, 8 and 9 migrated closely in one isolate, whereas segment 9 migrated separately from 7 and 8 in another sample (Savita et al. 2008a). Virus isolation in cell culture is useful only for group A avian RVs. Virus isolation is not frequently used for diagnosis and it is extremely difficult to cultivate other rotavirus serogroups in cell cultures (Herring et al. 1982; McNulty et al. 1981, 1984; Yason & Schat 1985; Theil et al. 1986a; Kang et al. 1986; Lozano et al. 1992; Tamehiro et al. 2003; Rodriguez et al. 2004; Villarreal et al. 2006). Detection of avian rotaviral antigens in tissues using fluorescent antibody (FA) and immune EM requires specific antisera. However, these procedures may be used to identify specific serogroups (Saif et al. 1985; Theil et al. 1986c). Besides EM, PAGE and virus isolation, flocks could be checked for AvRV by group specific RV antigen-VP6 using enzyme-linked immunosorbent assay (ELISA) or by immunohistochemistry (McNulty 2003; Lublin et al. 2004). Commercially available ELISAs are used for diagnosis of group A RVs in mammalian and


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avian feces only. However, no ELISAs are available to detect RVs of groups D, F and G so far. Using staphylococcal protein-A, co-agglutination test has been used to detect AvRVs in fecal samples (Kang et al. 1985). However, negative contrast EM has been found more sensitive than a staphylococcal protein-A coagglutination test (87%) and commercial ELISA (90%) for detection of group A RVs from turkeys and mammals. With clinical history of diarrhea along with high mortality, Legrottaglie et al. (1997) isolated three RVs from a 6 8-day-old flock followed by the characterization of RVA of avian origin by immune enzymatic (ELISA) technique as well as PAGE. While considering molecular detection tools for RVA, best option is highly rapid and sensitive reverse transcription-polymerase chain reaction (RT-PCR) (Guy 1998; McNulty 2003; Otto et al. 2006; Schumann et al. 2009; Trojnar et al. 2009, 2010; Kattoor et al. 2014). Rotaviral VP7 gene can be detected in fecal samples by PCR following conduction of a non-serotypable monoclonal antibody based ELISA (Gouvea et al. 1990; Watzinger et al. 2006). Use of RT-PCR has helped detection of RVs of turkey (Pantin-Jackwood et al. 2007, 2008). By use of recombinant technology, using Thermus thermophilus (rTth), a real-time RT-PCR (qRT-PCR) assay has been standardized. Use of rTth polymerase is proven to be advantageous as it does not require rotaviral doublestranded RNA denaturation before setting up an assay. A diverse number of AvRVs can be detected by employing such assay targeting NSP3 of virus in fecal samples (Mijatovic-Rustempasic et al. 2013). Some workers have developed a multiplex (m) RT-PCR assay, which could differentially detect presence of AsTVs (turkey astrovirus-2) and AvRVs in feces of birds (Day et al. 2007; Jindal et al. 2012; Day and Zsak 2013; Reck et al. 2013). Otto et al. (2012) detected avian RVs of group A (58.8%) and group D (65.9%) using a more sensitive and group specific real-time-PCR. To detect as well as to confirm RVA and RVD groups in avian species, a two-step RTPCR assay based on consensus VP6 gene of RVs is proposed (Kattoor et al. 2013a). Aside to detection, for molecular characterization of the AvRVs, genomic variations have been assessed by PAGE technique, RNA-RNA hybridization or by sequence analysis of virus genes (Theil et al. 1986b; Kang et al. 1986; Minamoto et al. 1991; Nishikawa et al. 1991; Ito et al. 1997, 2001; McNulty 2003). Sequencing of VP7, VP4 and VP6 genes assist molecular characterization of AvRV isolates and could be used to differentiate between turkey and chicken RVs (Ito et al. 1997), avian and mammalian RVs (Ito et al. 1995; Rohwedder et al. 1995; Trojnar et al. 2009) or may help in whole genome analysis of AvRV that could clearly give a vivid picture of features of AvRV isolates (Ito et al. 2001). Limited information exists regarding serotypes; but there are reports of identification of G7 serotypes among AvRVs (Nishikawa et al. 1991; McNulty 2003). Further characterization of VP7 and VP4 genes of AvRV isolates could give much idea regarding additional serotypes that might exist in poultry environment (Hoshino and

Kapikian 1996). Otto et al. (2012) for the first time applied sensitive RT-PCR assay targeting VP6-encoding genes of AvRV-A for detection of both AvRV-A and AvRV-D. Scanning as well as immune EM, Dot-ELISA along with hemagglutination test have been used for detection as well as molecular characterization of AvRVs belonging to RVD. A specific oligonucleotide primer set has been used for amplification of conserved region in RVD that has shown high degree of identity of viruses depending upon VP-6 gene (Hemida 2013). Primers have been designed specifically for gene encoding VP-6 protein in a RT-PCR. Up to a dilution of 5£10¡4 ng/mL of VP6 gene of RVD has been detected by PCR assay. This assay has been found to be highly suitable for rapid detection of RVD (Bezerra et al. 2012). Sequencing of VP7 genes have shown that pheasant RVs in Hungary are to be taken into consideration as representatives of a new specificity of VP7 genotype which has been designated as G23 (Ursu et al. 2009). Comparative sequence analysis has been done to reveal rate of homology of VP6 gene of RVD prevalent in various parts of the globe and northern India (Tarai area of the temperate western Himalayan region of India) (Kattoor et al. 2013b). Advances in field of diagnosis for development of sensitive and specific LAMP (Loop-mediated isothermal amplification of DNA) assay, recombinant protein based diagnostics, biosensors, biochips, microarrays, and nanodiagnostics need to be explored to their full potential for diagnosing avian RVs. Availability of next-generation sequencing as a new research tool has aided in exploring novel viruses at subtle level, cracking long-standing anonymities relating to genetically diverse and rapidly evolving enteric viruses. This metagenomic approach has been employed in several studies identifying potential zoonosis. Trojnar et al. (2010) first documented complete genome sequence of RVDs using sequence-independent amplification strategies and degenerate primers. Stucker et al. (2015) reported first complete genomic sequence for group G avian rotavirus (RVG) from South Africa using a sequence-independent amplification technique. These RVG genomes are highly diverse, especially in their VP4, VP7, NSP4 and NSP3 segments, indicating that RVG diversity is comparable to that of rotavirus A. 12. Differential diagnosis Rotaviral enteritis in poultry must be differentiated from other enteric pathogens causing diarrhea. Diarrhea as a clinical outcome is common to be caused by viral (adenovirus, reovirus, enterovirus, AsTV, CoV and paramyxovirus), bacterial (Salmonella, E. coli, Enterococcus) and protozoal (Eimeria spp. and cryptosporidium) enteric pathogens compared with rotavirus (Andral et al. 1985; Saif et al. 1985; Reynolds et al. 1987; Gough et al. 1990; Perry et al. 1991; Hines et al. 1995; Pascucci & Lavazza 1994; Yu et al. 2000; Jindal et al. 2009, 2010; Koo et al. 2013). Owing to clinical signs and pathology, RV disease does not essentially result in clinical disease (McNulty 1997, 2003; Tamehiro et al. 2003) and thus, laboratory diagnosis is essential.



13. Prevention and control For control of disease, initially secondary bacterial enteritis has to be kept under control through antimicrobial medication. To overcome dehydration, use of electrolyte solution is beneficial during acute stages of disease. Effect of diarrhea can be reduced in flocks by increasing ventilation rate, temperature or by adding fresh litter in poultry houses; as re-use of litter is considered an important reason for persistence of RV disease in flocks (McNulty 2003). Ubiquitous presence of RVs in turkeys and chickens, and their resistance to inactivation makes it difficult for a complete eradication (Guy 1998). Thus, in order to reduce environmental contamination and degree of exposure of young birds to RVs, control should aim at ensuring thorough cleaning and disinfection of poultry houses. Few published literature are available regarding susceptibility of avian RVs to chemical and physical inactivating agents. Heating of turkey rotavirus at 56 C for 30 minutes decreased infectivity to 100%, both in presence or absence of magnesium ions (Kang et al. 1988), but duck rotavirus was less stable to heat in presence of magnesium ions (Takase et al. 1986). Glutaraldehyde had greater inactivating capacity against AvRV than sodium hypochlorite and iodophor disinfectants (Minamoto & Yuki 1988). RVs are also sensitive to phenol and formaldehyde (Takase et al. 1986; Kang et al. 1988; Minamoto et al. 1988; Minamoto & Yuki 1988). Strict biosecurity measures must be followed in order to prevent any chance of spread of disease from one flock to another (Attoui et al. 2012). Frequent removal of litter and thorough cleaning of poultry house and equipments before restocking with a new flock could minimize the chance of disease. Rotavirus can be inactivated by heat at a temperature of 50 C for 30 min (Chmielewski et al. 2011). So, heat treatment can be done to samples or materials suspected for rotaviral contamination.

13.1. Vaccination It has been well proven that maternally derived antibodies have a paramount role in protection of intestinal mucosa against avian RVA attack, especially during the initial few weeks of life (Shawky et al. 1993; 1994; Saif & Fernandez 1996). As a consequence, vaccines have to be developed and should be made commercially available. Research on animal models showed that protection against rotaviral disease can be achieved by passive immunization, T cells or active immunization by vaccination (Desselberger & Huppertz 2011). Till to date, as it is difficult to develop vaccines largely due to high antigenic variation of AvRVs and the fact that non-RVA are difficult to grow in cell culture, such vaccines are not in practice. However, some workers have tried to develop inactivated vaccines against AvRVs along with experimental studies (Gough et al. 1999). Administration of inactivated vaccines to breeders are unlikely to protect progeny against challenge for more than the first week of life, unless much higher titers of anti-rotavirus antibody can be produced (Shawky et al. 1994; Gough et al. 1999). Besides vaccination, antibodies derived from eggs of

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immunized hens may be a less expensive and more practical alternative (Sarker et al. 2001). Oral administration of immunoglobulins isolated from eggs of immunized hens has been shown to prevent development of RV gastroenteritis in experimentally infected animals (Yolken et al. 1988). The long-term persistence of a high antibody level in yolk and simplicity of generation of large amounts of chromatographically pure antibody preparations may open new ways for their employment as an effective strategy to defend AvRV diseases. It has been shown that a fragment of monovalent antibody (recombinant), antirotavirus protein (ARP1), can lead to neutralization of disease in a mouse model. In vitro neutralization of a wide variety of serotypes or genotypes of RVs (including avian RVs) is done both by ARP1 as well as anti-rotavirus protein 3 (ARP3). ARP1 is a secreted protein while ARP3 is a 46 kDa surface-anchored protein (Aladin et al. 2012). ARP1, a rotavirus-specific antibody fragment isolated in 2006, derived from llama heavy chain antibodies (VHH fragments) can be used to neutralize rotaviral antigens. These heavy chain fragments were shown to be highly stable, efficiently produced in yeast and exhibiting high epitope specific affinity (van der Vaart et al. 2006). The viral enterotoxin, NSP4 is another option for vaccines as the NSP4 antigenic structure is highly conserved among RVs and is a good candidate for vaccine development (Borgan et al. 2003). Due to high risk of vaccine associated side effects, live attenuated vaccines in humans have been discontinued. Alternatives include virus particles (Jiang et al. 2013), virus-like particles (VLPs) (Azevedo et al. 2013), and DNA-based vaccines (Herrmann et al. 1996; Dhama et al., 2008) that are being explored for a fruitful outcome. Rotavirus VP6 nano-tubules combined with norovirus VLPs are used as novel candidate for RV vaccines (Tamminen et al. 2013; Pastor et al. 2014). VP6 specific single chain antibodies raised experimentally in llamas have been shown to have some cross-protective action in vitro and in vivo (Garaicoechea et al. 2008). Detailed studies on immune response of birds to rotavirus disease are insufficient and research studies regarding vaccine aspects are lacking. Two new generation RV vaccines, RotaTeq and Rotarix have been introduced on the global market for human RV. However, such groups of vaccines need to be developed for animal and avian RVs. Advances in generation of plant based edible vaccines, reverse genetics vaccines, vector vaccines, protein/peptide vaccines, reassortant vaccines, and vaccine delivery systems may be exploited for developing effective, safer and novel vaccines for countering AvRVs.

14. Therapeutic advances 14.1. Avian egg antibodies Currently, considerable research work has been done in chicken egg yolk antibodies (IgY) to be used as immunotherapeutics and diagnostics. The unique immunoglobulin molecule of chicken IgY is functionally homologous to mammalian IgG (Warr et al. 1995). Serum antibodies of


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chicken IgY are transferred from hens to embryo via egg yolk. Laying hens immunized against different antigens, transfer high concentration of specific IgY to egg yolk. Many researchers evaluated a beneficial effect of purified IgY antibodies specifically produced against RVs (Kuroki et al. 1993; Ebina 1996; Sarker et al. 2007; Buragohain et al. 2012; Diraviyam et al. 2014). Oral administration of chicken IgY has been shown to be effective against diarrheal pathogens in various animals and humans especially against bovine and human RVs. However, the main disadvantage is the stability of IgY in the GI tract. Exploring an effective method to prevent degradation of antibodies in GI tract would form a basis for significant immunotherapeutics and nutraceutical applications of IgY (Mine & KovacsNolan 2002). Obviously, no published information is available regarding the role of avian egg antibodies (IgY) as immunotherapeutics and diagnostics against avian RVs. In future, research on IgY will offer a great platform for formulating prophylactic strategies against AvRVs. 14.2.

Herbs and essential oils as antiviral agents

Herbs and herbal extracts are gaining tremendous attention as antibacterial and antiviral agents. Various herbs have been studied for their potential as antiviral agents against human RV disease (Taherkhani et al. 2013). Experimental study with herbs like Stevia rebaudiana, Alpinia katsumadai, Citrus aurantium, soy isoflavones, Achillea kellalensis Boiss and black tea revealed in vitro activity against human RV and found to be effective to prevent infection with minimal toxicity (Andres et al. 2007; Kim et al. 2012). Various essential oils are being used as antimicrobial agents (Li et al. 2013; Gopi et al. 2014; Giannenas et al. 2014). Recently, bio engineered probiotics are also being studied for their efficacy to prevent rotaviral and other enteric diseases. Similar studies are lacking for avain RVs and thus, needed to know their efficiency against AvRV disease (Amalaradjou & Bhunia, 2015). Cinnamon and its oil have been documented to be effective against RV in man that needs attention against AvRVs (Ranasinghe et al. 2013). Attention needs to be given also for utilizing novel and alternative/complementary immunomodulatory and treatment modules including cytokine therapy, si-RNAs, toll like receptors, phages, avian egg antibodies, probiotics, nutritional immunomodulation, herbs and nanomedicines to prevent and treat AvRV diarrhea (Dhama et al. 2013, 2014; Mahima et al. 2012, Malik et al. 2013b; Tiwari et al. 2014). 15. Conclusion and future perspectives Due to co-circulation of different genotypes within an area, rotavirus group A diseases have intricate epidemiology. Changes can occur in viral genome due to accumulation of point mutations and gene reassortment (genetic shift), enabling AvRVs to exhibit significant antigenic variation. Both these phenomenon are playing a key role in generating ample diversity among RVs. Sequence and phylogenetic analysis further confirm the sequence

diversity and varying evolutionary dynamics of AvRVs in birds. The increasing popularity of viral metagenomics, using different high-throughput sequencing platforms to detect viral diversity in clinical, pathological and environmental samples, are further expanding our knowledge on these highly diverse AvRVs. To determine ecology of RV disease, special attention is needed to be given as far as epidemiology (including the molecular epidemiology) of AvRVs are concerned especially in case of wild birds. Improvement in molecular diagnostic assays and allied techniques are quiet noteworthy for early and accurate diagnosis of AvRVs. Novel detection tools have to be developed and judiciously employed, so that a rapid diagnosis is facilitated. There is still need for pen side high throughput diagnostic arrays for on-site detections of causative agents. Development of vaccines may help in countering persistence of virus in the environment via bird excretion to a moderate level. Development of new generation vaccines using immunogenic antigens of AvRV has to be explored and given due importance. Till now, no effective vaccines are available to control AvRVs. Even though it is difficult to completely get rid of RVs from poultry environment, adoption of strict sanitation and hygienic measures could favor in subsiding its occurrence, spread and incidence in poultry flocks minimizing ultimately losses associated with RV disease. Acknowledgements The authors are highly thankful to DBT and ICAR Projects, Delhi for strengthening facilities for research at IVRI, Izatnagar.

Disclosure statement The authors declare that they have no competing interests.

ORCID Kumaragurubaran Karthik 6306

http://orcid.org/0000-0002-9215-

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