Rotavirus infections

Previous authors: A D STEELE, A GEYER AND G H GERDES

Current authors:
J O AMIMO - Lecturer, DVM, MSc, PhD, Animal Production, University of Nairobi, P.O. Box 29053, Nairobi, 00625, Kenya
A N VLASOVA - Assistant Professor, PhD, DVM, The Ohio State University, 1680 Madison Ave, Wooster, Ohio, 44691, USA
L J SAIF - Professor, MS, PhD, Food Animal Health Research Program, CFAES and CVM, OARDC, The Ohio State University, 1680 Madison Ave, Wooster, Ohio, 44691, USA

GENERAL INTRODUCTION: REOVIRIDAE

Introduction

Rotaviruses are ubiquitous in nature and generally cause infection of the small intestine in the young of many mammal and bird species.⁵⁰ The disease occurs predominantly in intensively reared animals and is characterized by acute disease, a short incubation period, anorexia and diarrhoea.

Rotavirus infection was first recognized in 1963 in mice,² followed by isolation of the SA11 (simian agent 11) in vervet monkey cell culture.^{18, 96} In 1969 virus particles (70 nm in diameter) were detected in bovine faeces and were shown to be associated with diarrhoea in calves.¹¹² These murine,¹¹⁹ simian and bovine agents were later found to share a common group antigen and to be morphologically indistinguishable by transmission electron microscopy (TEM). Bovine rotaviruses (BRV) were among the earliest rotaviruses to be successfully adapted to cell culture¹¹⁰ after which research efforts were directed toward their characterization.

Rotaviruses have a world-wide distribution and commonly affect calves,^{111, 169} lambs,^{107, 156} piglets,^{14, 137, 144} goat kids⁴¹ and foals.^{39, 41}

Aetiology

Rotaviruses are now classified in the family Reoviridae, genus Rotavirus,^{44, 50, 102} and each rotavirus is named after the species in which it occurs.They have a distinct morphology, revealed by TEM of negatively-stained virus in faeces (Figure 1). Those from different species and serogroups are morphologically indistinguishable, i.e. a non-enveloped virion with icosahedral symmetry.⁵⁹ Three types of particles are evident: viral cores, double-layered and the triple-layered, with the latter constituting the complete infectious particle.

The name rotavirus derives from the Latin ‘rota’ meaning wheel⁵⁹ because the outer capsid has a sharply defined outline resembling the rim of a wheel approximately 70 nm in diameter.²⁴ The double-layered particle or inner capsid particle is approximately 55 nm in diameter⁵⁰ while the electron-dense core is hexagonal and approximately 37 nm in diameter.⁵⁸

The rotavirus genome is composed of eleven segments of double-stranded RNA encoding six structural (VP1–VP6) and six nonstructural (NSP1–NSP6) proteins.⁵⁰ The segments can be readily separated by polyacrylamide gel electrophoresis (PAGE) producing a characteristic pattern known as an RNA electropherotype.¹⁴⁵

The dsRNA segments can be divided into four class sizes (I to IV) based on migration through PAGE. Group A rotaviruses have a characteristic 4-2-3-2 PAGE pattern which is generally conserved among these viruses. However, groups B and C rotaviruses, which are also found in most domesticated livestock, have distinct patterns that allow rapid differentiation of strains from different serogroups.^{7, 132, 158} The group B rotaviruses have a characteristic RNA electropherotype where the segments cluster in a 4-2-2-3 pattern, and the group C rotaviruses exhibit an electrophoretic pattern of 4-3-2-2.^{132, 158} The viruses from the different serogroups of A, B and C rotaviruses also have distinct group antigens (see below) that induce non-cross-reactive antibody spectra.

Among livestock species, group A rotaviruses have been implicated in acute gastroenteritis in piglets, lambs, calves, foals, chickens and turkeys.^{21, 31, 132, 158} Additionally, rotaviruses from groups B and C have been recovered from the faeces of piglets, lambs, calves and foals.^{32, 158}

Figure 1 Rotavirus particles viewed by transmission electron microscopy in a faecal filtrate from a calf with diarrhoea

Considerable antigenic diversity is found among rotaviruses and, historically, isolates were classified into groups based on the viral protein 6 (VP6) antigenic characteristics. They are further subdivided into dual serotype specificities (serotypes) and genotypes on the basis of outer capsid antigens/genes VP7 and VP4 (Table 1). To date, rotaviruses have been classified into at least nine groups/species (designated as RVA–RVI) on the basis of differences in the antigenicity of their middle capsid VP6 protein and nucleotide sequence identities of the VP6-encoding gene.^{100, 106, 117} A tentative tenth group (RVJ) was reported in bats.⁹ Among the nine RV groups, RVA, RVB, RVC and RVH are found in both humans and animals, while RVD–RVG have been detected only in animals, including birds, so far (Table 1).

Rotaviruses belonging to the RVA group are the most common cause of viral diarrhoea in a wide variety of animal species and birds and the most diverse group both genetically and antigenically due to point mutations and reassortment of cognate genes.¹⁰⁵ However, most recent data also show a significant diversity of RVB and RVC in pigs.^{6, 97, 101} Thus group A rotaviruses from calves, lambs, piglets and human infants share common or related antigens that are cross-reactive amongst these strains. These are distinct antigenically and by gene sequence from the VP2 and VP6 proteins of the group B or C rotavirus strains.

The major dual classification of rotaviruses (serotypes) is based on the VP7 and VP4 outer capsid antigens. Viral protein 7 (VP7) contains the major neutralizing antigen of the virus and is an important consideration in the selection of viruses for inclusion as vaccine candidates. The VP7 serotypes are distinguished by various neutralization assays such as plaque neutralization⁷⁹ and monoclonal antibody based enzyme-linked immunosorbent assay (ELISA).¹⁵⁵ Molecular techniques based on the viral genomic RNA such as reverse transcription-polymerase chain reaction (RT-PCR) and hybridization are used to detect and differentiate the VP4 and VP7 genotypes within each RV group.

Thus far, at least 28 VP7 genotypes (G-types) and 39 VP4 P genotypes have been reported in the highly genetically diverse group A rotaviruses (Table 2), representing a continuous challenge for vaccine development.¹⁴¹

The dual (G/P) typing system was extended in 2008 to a full-genome sequence classification system, with nucleotide per cent identity cut-off values established for all 11 gene segments , with the notations Gx-P[x]-Ix-Rx-Cx-Mx-Ax-Nx-Tx-Ex-Hx used for the VP7-VP4-VP6-VP1-VP2-VP3-NSP1-NSP2-NSP3-NSP4-NSP5/6 encoding genes, respectively,¹⁰⁴ with "x" indicating the numb,/er of the genotype. For example, Wa human RVA is classified as G1-P[8]-I1-R1-C1-M1-A1-N1-T1-E1-H1, OSU porcine RVA is classified as G4-P[6]-I1-R1-C1-M1-A8-N1-T1-E1-H1, while UK (tc) bovine RVA strain is G6-P[5]-I2-R2-C2-M2-A3-N2-T7-E2-H3.

The discovery that viral infectivity was enhanced by the addition of proteolytic enzymes such as pancreatin and trypsin to the  cell culture growth medium aided in the isolation of these viruses.⁷ Use of an embryonic African green monkey kidney cell line (MA-104) with the incorporation of trypsin to the maintenance medium and the use of roller cultures has enabled the routine isolation of most animal RVA but only a few RVB¹⁷⁰ and RVC.¹⁶⁸

Rotaviruses are stable within a pH range of 3 to 9, in the presence of ether and chloroform and are not easily inactivated. They are resistant to iodophor and quarternary ammonium disinfectants and show an unusually high resistance to inactivation by products containing chlorine and sodium hypochlorite. Ethanol, phenol, formalin and lysol are useful disinfectants.^{157, 166} In practice 37 per cent formaldehyde diluted 1:10, 0,75 per cent hexachlorophene diluted 1:3, and 67 per cent chloramine T with 16,4 per cent chlorine diluted 1:5 are effective in destroying the virus.

Epidemiology

In calves infection usually occurs from week two to 11 of life but is rare in the first week after birth.^{23, 54} Although the infection rate may be as high as 79 per cent in calves,⁴² the proportion of animals that actually develop disease varies.^{42, 108} The role of non-group A rotavirus infections in calf diarrhoea is unclear although a high proportion of suckled calves have antibodies to group B and C rotaviruses.^{20, 26}

Table 1 Genetic diversity of rotaviruses

*Provisional classification

Table 2 VP7 serotype specificity of group A rotaviruses and the species of origin and prevalence

Rotavirus infections cause important economic losses related to deaths, reduction in weight gain and treatment costs of affected animals. Neonatal calf diarrhoea virus (NCDV) and UK bovine prototype strains have been established as G6, whereas B223 and KK-3 are G10.^{86, 169} G6, G8 or G10 RVAs possessing VP4 genotype P[1], P[5] or P[11] are commonly found in cattle, with G6P[5] being the dominant genotype combination among bovine RVAs.^{103, 127} In addition, investigators have reported that the G/P types may vary among beef and dairy cattle, with G6 dominant in beef and G10 dominant in dairy cattle.⁹⁴ Other VP7 genotypes (G1–G4, G5, G11, G12, G15, G17, G21 and G24) and VP4 genotypes (P[3], P[6], P[7], P[14], P[17], P[21], P[29] and P[33]) have been reported occasionally in cattle. Detection of rotavirus serotypes G1, G2, G3, and G11 in faeces of diarrhoeic calves by using polymerase chain reaction-derived cDNA probes has been reported.⁸⁰ Among the bovine RVAs with novel genotypes, the G21P[29] and G24P[33] strains were isolated from asymptomatic cows.¹ Strains RVA/Cow-wt/JPN/Azuk-1/2006/G21P[29] and RVA/Cow-wt/JPN/Dai-10/2007/G24P[33] appeared to be more closely related to simian or canine/feline rotaviruses than bovine rotaviruses, pointing toward possible interspecies transmission and multiple reassortment events involving bovine, simian and canine/feline RVAs.

Ovine RVs are members of either RVA or RVB, but the epidemiology of lamb RVs is still largely uncertain. The occurrence of ovine RVAs has been reported in various countries worldwide with detection rates up to 60 per cent, often with estimated 10 to15 per cent mortality rates. Limited information is available on genotypes of ovine RV strains globally. In India the most prevalent RVA VP7 genotype is G6 followed by G10, while the prevalent VP4 genotype is P[11].⁶¹ In China only G10P[15] RVA has been detected in sheep, while G10, G3 and G6 were reported to be prevalent in Spain. In the United Kingdom four lamb RVA strains were characterized, each one showing different specificities, namely G3P[1]; G6P[11]; G9P[8] and G10P[14].⁵⁶

The occurrence of caprine RVA and RVB has been reported from various countries worldwide. The prevalence of RVA in goats reported in different countries was ~60 per cent in Italy, and  8 per cent and 50 per cent in Spain. Very few epidemiologic studies of RV in goats have been reported in Africa or Asia.

Information on the genotypes of caprine RVA strains globally is limited. Genotypes G6P[1] were reported in Italy and Bangladesh, G6P[14] in South Africa, G3P[3] in Korea, G10P[15] in China, G8 in India and G6P[1] or G8P[1] in Turkey.^{5, 63, 89, 136} Older lambs are less susceptible than new-born animals to ovine rotavirus but the disease is clinically mild even in lambs less than 10 days old unless aggravated by stress or secondary bacterial infections.¹⁵⁹ Non-group A rotaviruses, which may be more common than other rotavirus types, may also be associated with acute fatal enteritis of young lambs.³¹

Rotaviruses of the RVA group are the main cause of diarrhoea in foals up to three months of age, causing severe economic loss due to morbidity and mortality. Equine RVA strains were first detected in foals with diarrhoea in England in 1975.⁵⁷ Within the equine RVA, G3 and G14 are the most common VP7 genotypes worldwide and are always associated with the P[12] VP4 genotype.^{37, 49, 124, 128} In addition, a limited number of porcine-, bovine- and feline-like RVA viruses have been detected in horses^{36, 57, 85, 167}. In a survey in the USA, rotavirus was found in the faeces of 30 per cent of diarrhoea cases in foals,³⁹ but the majority of infections were probably subclinical and were not diagnosed. Seroprevalence studies have shown that almost 100 per cent of animals develop antibodies to rotavirus.²⁰ In foals infection occurs from three days to three months of age.³⁹ Rotavirus antibodies disappear from mares’ milk within seven to 16 days of parturition, and loss of maternal antibodies influences susceptibility of the foal to subsequent infection.³⁹ Large fluctuations in ambient day and night temperatures and crowding of calves are important factors that predispose to outbreaks of the disease.¹²⁰ Stress and secondary infections with a variety of agents contribute to the severity of the disease.⁵¹  Rotavirus infection in calves and piglets may potentiate the effects of Escherichia coli and vice versa.¹⁷³

Porcine rotavirus (PRV) infection is endemic in pig herds worldwide.¹⁷⁶ Antigen detection studies showed that two-thirds of herds are infected with PRV,¹⁴ while sero-prevalence studies indicated that almost 100 per cent of animals have been exposed.¹⁶ Of the nine RV groups (A-I), RVA, RVB, and RVC are associated with diarrhoea in piglets. Although discovered decades ago, porcine group E RVs (RVE) are uncommon and their pathogenesis has not been well studied. Many rotavirus infections in piglets are subclinical or result in mild diarrhoea lasting one to three days only,¹⁰ and diarrhoea caused by RVA is uncommon in the first week of life. Clinical disease is usually observed at one to two weeks of age and up to three to five days post-weaning.^{14, 88} Rotavirus C and A shedding and disease occur in nursing (one to two weeks of age) and weaned piglets, respectively.^{14, 40, 177} Reports of mortality are variable and range from seven to 20 per cent in nursing piglets and three to 50 per cent in weaned pigs.¹⁴ Recent studies have shown a high and increasing prevalence (up to 78 per cent) of RVC infection in the USA, Ireland, South Korea and Italy.^{6, 38, 82, 97, 99} Furthermore, in the USA the prevalence of RVC infection was higher than for RVAs in  diarrhoeic piglets over three weeks of age.^{6, 99} In piglets, the most common rotavirus serotypes are G3, G4, G5 and G11.^{16, 79, 123, 146} Porcine rotavirus serotypes G4 and G5 strains have been isolated globally with G3 strains from Australia¹²³ and Latin America.³⁵ The porcine serotype G3 and G4 strains are antigenically related to the human rotaviruses of the same VP7 serotype. There have been reports of human-like RVA genotype G1 strains in calves,¹² and G1 and G2 strains in piglets,¹³¹ although the significance of these strains in nature is unclear.

Infection occurs via the faecal–oral route by exposure of susceptible animals to faeces of infected individuals or to fomites. Transmission of the disease is favoured by the presence of large amounts of virus in diarrhoeic faeces (10¹¹/g) and resistance of the virus to environmental conditions. These factors ensure rapid and heavy contamination of the surroundings as well as survival of the virus for prolonged periods.

Cows and sows may excrete virus in the faeces at the time of parturition and provide a source of infection for their offspring.¹¹ However, the usual mode of spread is from neonate to neonate. Experimentally infected calves excrete the virus by the second day of infection and continue to do so for seven to eight days. Under natural conditions rotavirus may be present in the faeces of young animals from three days after birth.^{11, 42}

Pathogenesis

The outcome of infection in all species depends on the virulence of the viral strain, the quantity of virus ingested, the presence of maternally derived antibodies in the lumen of the gut at the time of exposure,^{14, 30} age-related resistance to the disease.^{22, 143, 172} and animal management practices. The pathogenesis of RV infections also depends on virus-host interactions and viral gene products (VP3, VP4, VP7, NSP2, NSP3, NSP4).^{8, 25, 28, 71, 77, 78, 139} Infection occurs shortly after birth but is usually subclinical in the presence of colostral antibodies in the gut.

The virus has an affinity for mature enterocytes at the tips of the villi of the small intestine. As a result of infection, these cells, which have an absorptive function, are desquamated more rapidly than usual and are rapidly replaced by undifferentiated epithelial crypt cells, which have a secretory function.^{45, 118} Crypt cells lack sucrase or disaccharide enzyme function, leading to inability to utilize lactose. D-xylose malabsorption also occurs as a result of the loss of differentiated enterocytes.¹⁸³ Undigested carbohydrates in the lumen of the colon are broken down by fermentation bacteria to short-chain fatty acids, giving rise to a hypertonic solution and subsequent osmotic fluid loss.

As a result of damage to the epithelium, the cellular sodium transport system is also disturbed, resulting in a net flow of fluid from the extracellular space into the lumen of the gut. The total faecal output is thus markedly increased with a concurrent loss of Na⁺ and Cl⁻ ions.¹¹⁵ Animals may die as a result of fluid loss, electrolyte imbalance and concomitant acidosis if appropriate therapy is not instituted.¹⁷⁹ Inflammatory changes in the intestine may cause hypermotility and aggravate the diarrhoea.^{40, 179} Colonization of the bowel by other infectious agents such as E. coli and Salmonella serovars increases the severity of the condition.^{51, 173, 182} Extra-intestinal spread of RV also occurs frequently as shown by detection of RV dsRNA, RV antigen or infectious RV in serum and other body sites.^{13, 83, 95, 153} However, the significance of the extra-intestinal occurrence of RV in causation of disease is controversial.^{52, 138, 140} It has been shown that RV can replicate in the liver, the biliary system and the pancreas, leading to biliary atresia and pancreatitis in immunocompromised murine hosts.^{53, 64} More recently, vomiting in RV-infected human hosts was explained by the fact that RV can infect the enterochromaffin cells in the gut, stimulating production of serotonin, which activates the afferent fibres of the vagus nerve and stimulates the brain stem sites controlling vomiting.^{72, 73}

 An immune evasion mechanism by rotaviruses, mediated by down regulation of interferons and other cytokines, was suggested based on gene expression profiling using microarrays⁴

Clinical signs

Rotaviral diarrhoea is usually sporadic in occurrence since most infections are in suckling animals with maternal immunity and thus most infections are subclinical. However, in situations with limited or no transfer of maternal immunity or after loss of maternal immunity (weaning) and where other predisposing factors occur simultaneously, the prevalence of disease may reach epidemic proportions.

The incubation period is generally 18 to 96 hours. Affected animals are initially depressed, reluctant to move and anorectic.^{181, 182} This is followed by profuse diarrhoea, dehydration and loss of body weight. Diarrhoea may be prolonged, up to 14 days in piglets, and severe if the animal recovers sufficiently rapidly to recommence feeding.^{14, 90, 181}  The colour of the faeces depends on the diet and varies from yellow or brownish-grey to light green and seldom contains blood or mucus, unless secondary bacterial infection occurs.^{159, 182} It is usually an afebrile disease unless complicated by secondary bacterial infection. Affected animals may die as a result of dehydration, electrolyte imbalance and secondary infections.^{179, 182}

Pathology

The only macroscopic changes in animals that have succumbed to this infection are dehydration, an increase in the fluid content of the gut, and presence of diarrhoeic faeces accompanied by contamination of the perineum and hind legs by faeces. Upon necropsy, intestinal walls are thin and filled with yellow fluid. The stomach may be full of undigested milk.

Microscopic changes are largely confined to the villi of the small intestine.^{111, 133} The cranial portion of the duodenum is generally not affected and there is a patchy distribution of affected areas throughout the rest of the small intestine.  Villi appear blunt, short and fused, giving the mucosa an almost avillous appearance.¹³³ Shortening of the villi is due to the loss of brush-border columnar epithelial cells, which are replaced by cuboidal or squamous cells lacking a brush border from the crypts. Increased numbers of mononuclear inflammatory cells may occur in the lamina propria.^{111, 164}

Immunofluorescence studies showed that viral antigens are confined to the cells at the tips of villi in the middle and posterior small intestine of calves and piglets.^{15, 135} These cells are shed for 18 to 96 hours after infection.^{40, 154} In lambs, antigen is also present in the enterocytes of the large intestine, but less abundantly than in the small intestine.¹⁵⁹ Within infected cells, the virus is associated with the cisternae of the rough endoplasmic reticulum.¹²⁹

Diagnosis

Diagnosis of rotavirus infection is based on the detection of large numbers of viral particles in the intestinal contents or faeces^{76, 148, 165} by TEM. Virus isolation was once considered the 'gold standard' for detecting viral pathogens in samples; however, more rapid and sensitive methods are currently available including ELISA and RT-PCR. Cell culture is used to isolate viruses for diagnostic purposes as well as virus propagation for vaccine development or virus genetic characterization. Moreover, it is notable that field strains of RV may fail to replicate in vitro, and especially RVB and RVC.  Many cell lines (e.g. MDBK, MA104, TF and PK-15 cells) have been used to isolate RV from animal faecal samples. Viral isolation has three advantages including:

1. confirmation of the presence of the virus in a clinical sample,
2. availability of the isolated virus for further genetic characterization and development of diagnostic kits and vaccine, and
3. does not require virus/strain specific reagents except for confirmation of the virus isolate.

However, besides overall failure to grow in vitro, there are also several downsides to viral isolation including low sensitivity, variable permissiveness of cells, dependence on proper collection and handling of samples for virus viability and non-applicability for cytotoxic specimens.

Transmission electron microscopy  applied to negatively- stained faeces or intestinal contents is  commonly used for diagnosis because of high concentration of virus in clinical cases.¹⁰ This technique has the added advantage of demonstrating other infectious agents in cases of mixed enteric infections. There are two types of TEM: direct TEM and immune electron microscopy (IEM).^{17, 148} Two different staining techniques (positive and negative staining) can be performed to visualize the target. Immuno-electron microscopy has greater sensitivity than direct TEM since the specimen is incubated with antibody specific for the target virus in order to agglutinate the virus before staining. Most rotavirus geno-groups are difficult to isolate or propagate in cell culture (except group A rotaviruses) but can be differentiated easily from other pathogens according to their unique morphology by TEM.

Direct or indirect fluorescent antibody tests can be used to demonstrate antigen in cell culture, faecal smears and histological sections of the intestine.^{23, 112}

The occurrence of shared, group-specific antigens enables human rotavirus enzyme-linked immunosorbent assay (ELISA) kits, which are available commercially, to be applied to the screening of large numbers of faecal specimens for viral antigen.^{70, 122} However, generally these kits have not been validated for detection of animal RVs so their sensitivity/specificity are generally undefined. These assays may also be used for serological screening, although high antibody prevalence in most populations negates the diagnostic value of this approach. A rapid, highly specific, and sensitive antigen-capture enzyme-linked immunosorbent assay (AC-ELISA) has been developed for detection of porcine RVA, by using VP6 (a highly conserved and antigenic protein of group-A rotavirus)-directed rabbit polyclonal antibodies (capture antibody) and murine monoclonal antibodies (detector antibody),¹¹⁴ which is advantageous in large-scale surveillance, timely detection and preventive control of rotavirus infections in swine farms. Similar but also G type (VP7) -specific ELISA was developed for detection and G typing of bovine RVA from beef and dairy calves.⁹⁴

Other tests that were used historically for antigen detection include complement fixation, counter immuno-electrophoresis, radio-immunoassay and agar-gel diffusion; however, their use is less common nowdays.

Polyacrylamide gel electrophoresis (PAGE) of viral RNA extracted from faeces or virus propagated in cell culture is commonly used in epidemiological studies, particularly for differentiating between viral isolates and as a rapid means of detecting atypical rotaviruses in faecal specimens.^{34, 132, 145, 163}

Several molecular detection tools are  available. Hybridization tests have been developed using labelled cDNA probes based on hypervariable regions of outer capsid genes of RV that could characterize animal rotavirus strains.^{125, 130} RT-PCR using validated primers designed from RV genes is currently the most widely used assay for detection of RVs in animals.^{6, 62, 66-68, 81, 98, 126} Additionally, semi-nested or multiplex RT-PCR has been developed and used for the same purpose.^{92, 93, 116} RT-PCR is highly sensitive and specific and is suitable for genotyping RV and it has become the gold standard for RV diagnostics.⁸¹ Methods like sequencing and oligonucleotide microarray hybridization that are sensitive and capable of discriminating mixed rotavirus infections are also available.

Differential diagnosis

The aetiological diagnosis of neonatal calf diarrhoea is difficult; a reliable diagnosis is impossible in up to 27 per cent of cases.¹⁷¹ A variety of infectious agents, including rotaviruses, coronaviruses, enterotoxigenic E. coli, and cryptosporidia, may cause diarrhoea in neonatal calves.^{142, 161} Laboratory assistance is thus necessary to arrive at a diagnosis.

Variation in the frequency of rota- and coronavirus detection in beef and dairy calves has been demonstrated, coronavirus being more commonly found in beef calves and rotavirus in dairy animals.²⁷

The differential diagnoses of enteritis in lambs include colibacillosis, salmonellosis, coccidiosis, cryptosporidiosis and adenovirus infections.

Diarrhoea as a result of rotavirus infection in foals should be differentiated from that caused by other infections such as E. coli, Salmonella serovars, Rhodococcus equi, Actinobacillus equuli and Clostridium spp., as well as foal-heat diarrhoea, nutritional factors and internal parasites.

The lesions and pathogenesis of porcine rotavirus diarrhoea closely resemble those of porcine transmissible gastroenteritis (TGE), porcine epidemic diarrhoea  (PED) or  porcine deltacoronavirus infection  caused by coronaviruses.¹³³ Porcine rotavirus diarrhoea should be differentiated from other causes of diarrhoea such as E. coli,  internal parasites and nutritional factors. A multiplex RT-PCR has been developed that is reportedly able to differentiate  TGEV,  PEDV and porcine  RVA.¹⁶³

Control

As death is due to dehydration, loss of electrolytes, acidosis and shock, treatment should primarily be aimed at rehydration and the correction of electrolyte imbalances. Depending on the degree of dehydration, fluid may be given orally or parenterally. Antibiotics may be administered to control secondary bacterial infection. Because of the stability of rotaviruses and the high concentration of virus in the faeces of infected animals, cases should be segregated from non-affected animals, cold-stress and indoor crowding should be avoided and calving/farrowing areas cleaned and rotated if possible. Rotavirus build-up may also occur in the vicinity of outdoor water troughs.

Measures should be taken to enable timely and sufficient ingestion of colostrum, the principal mode of protection. The presence of colostral antibodies in the lumen of the gut (not circulating antibody) is necessary for the protection of neonates.¹¹³ Levels of colostral IgG decline rapidly in the transition from colostrum to milk and, in cows, the amounts present by the second week after parturition are no longer protective.^{48, 162, 178} In sows secretory immunoglobulin (IgA) in milk provides protection and the level remains constant during lactation, but may not be protective if the RV infectious dose is high.¹⁴⁷ This differs from the situation in cattle, sheep and horses where colostral immunity is only protective for a short period (~5 days).

During outbreaks of neonatal diarrhoea in calves, the feeding of milk with 10 per cent colostrum from a colostrum pool provides passive protection for the two- to three-week period of risk.^{3, 47, 150} Thereafter the age-related resistance to clinical infection may provide sufficient protection of older animals. The feeding of artificial colostrum containing serum immunoglobulins, whey and vegetable oils or of IgY egg yolk antibodies¹⁷⁵ has been used with good results.¹²¹ This strategy is obviously only applicable in bucket-fed dairy calves. If insufficient colostrum is ingested by neonatal lambs, immune serum fed twice daily at 2,5 ml/kg will afford specific protection.¹⁶² To boost maternal antibody levels, the dams (cows and ewes) need to be immunized with RV vaccines a few weeks before parturition to enhance passive protection in neonates.^{3, 150, 165}

Oral immunization of calves less than one day old with an attenuated live virus vaccine elicits local cellular resistance.^{113, 174} Field trials with this vaccine have, nevertheless, been disappointing, as neutralization of vaccine virus by colostral antibodies occurs in the lumen of the gut, making the timing of administration crucial.^{43, 150}

An alternative approach is maternal vaccination of pregnant animals. This has been reviewed by Saif and Fernandez, 1996¹⁴⁹ and Chattha et al., 2015.³³ Intramuscular immunization of pregnant animals results in increased levels of IgG in the serum and consequently colostrum.^{29, 134} Studies using a combined inactivated rotavirus-enterotoxigenic E. coli vaccine with an adjuvant resulted in increased immunoglobulin content of colostrum and milk and prolonged passive lactogenic immunity in calves.^{151, 160} Similarly, the use of a commercial vaccine one to three months before calving significantly reduced the prevalence of rotaviral diarrhoea in an affected herd.¹⁰⁹ Although a number of VP7 serotypes of bovine rotavirus have been identified, vaccination of cows usually results in broad immunity with respect to serotype because of the heterotypic response of adult animals, which have usually been previously exposed to a variety of different serotypes. Supplementation with probiotics can prevent rotavirus-induced diarrhoea in young animals.⁶⁵

If available, a commercial vaccine containing inactivated rotavirus, coronavirus, Clostridium perfringens type C toxoid and K99 E. coli bacterin can be used in pregnant cattle. Two doses are administered two weeks apart, with the second administration two to three weeks before calving. Vaccination should always be accompanied by change in management incorporating attention to factors causing stress and, more particularly, good hygiene.

High immunoglobulin levels in cows’ milk lasting at least 30 days after calving were obtained by the intramuscular or intramammary vaccination of pregnant dairy cows nine weeks prior to calving and by the inoculation of modified live virus together with an adjuvant into the mammary gland two weeks later.^{151, 152}

Bovine colostrum has been used to protect piglets against rotavirus infection,^{19, 121, 160} although it was found that a vaccine prepared for cattle did not afford protection.⁹¹ A commercial porcine rotavirus vaccine has undergone field trials in the USA with variable results.^{60, 75, 87}

Past studies using recombinant DNA and subunit vaccines, plant-based edible vaccines and virus-like particle (VLP) vaccines demonstrated modest to good (2/4/6/7 VLP or combined virus and 2/6VLP vaccines) immunogenicity.^{46, 55, 69, 74, 84, 180}

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