Abstract
Rotavirus B (RVB) infection in cattle is poorly understood. The objective of this study was to describe the epidemiological features of repeated outbreaks of epidemic diarrhea due to RVB infection in adult cattle on a large dairy farm complex in Japan. In October 2002, approximately 550 adult cows and approximately 450 in February 2005 had acute watery diarrhea at several farms on the complex. Four months before the first outbreak, RVB antibody-positive rates at subsequently affected farms were significantly lower than at non-affected farms (30% to 32% versus 61% to 67%). During the acute phase of both outbreaks, RVB antibody-positive rates in diarrheal cows tested were as low as 15% to 26%. Most of the farms affected in the second outbreak were also involved in the first outbreak. Some adult cows with RVB diarrhea in the first outbreak showed not only RVB seroresponse, but also RVB shedding in the second outbreak, although none of these cows developed diarrhea. Nucleotide sequences of the VP7 and VP4 genes revealed a close relationship between RVB strains in both outbreaks. Taken together, these results indicate that outbreaks of epidemic RVB diarrhea in adult cows might be influenced by herd immunity and could occur repeatedly at the same farms over several years. To our knowledge, this is the first report on repeated RVB infections in the same cattle.
Résumé
L’infection par le rotavirus B (RVB) chez les bovins est peu comprise. L’objectif de la présente étude était de décrire les caractéristiques épidémiologiques de poussées de cas répétées de diarrhée épidémique dues à une infection par le RVB chez des bovins adultes dans un grand complexe laitier au Japon. En octobre 2002, environ 550 vaches adultes et environ 450 en février 2005 présentaient une diarrhée aqueuse aigüe dans plusieurs fermes sur le complexe. Quatre mois avant le premier épisode, les taux d’anticorps anti-RVB dans les fermes subséquemment affectées étaient significativement plus faibles que dans les fermes non-affectées (30 % à 32 % vs 61 % à 67 %). Pendant la phase aigüe des deux épidémies, les taux d’anticorps anti-RVB chez les vaches diarrhéiques testées étaient aussi bas que 15 % à 26 %. La plupart des fermes affectées dans la deuxième épidémie étaient également impliquées dans la première épidémie. Quelques vaches adultes avec une diarrhée à RVB dans la première épidémie avaient non seulement une réponse sérologique positive envers le RVB, mais excrétaient également le RVB durant la deuxième épidémie, bien qu’aucun de ces vaches ne présenta de diarrhée. Les séquences nucléotidiques des gènes VP7 et VP4 ont révélé une proche parenté entre les deux souches de RVB des deux épidémies. Pris globalement, ces résultats indiquent que les épisodes de diarrhée épidémique causée par RVB chez des vaches adultes peuvent être influencés par l’immunité du troupeau et peuvent survenir de manière répétée sur une même ferme pendant plusieurs années. Selon nous, il s’agirait du premier rapport de cas d’infections à répétition par le RVB chez les mêmes bovins.
(Traduit par Docteur Serge Messier)
Introduction
Rotaviruses (RVs) are members of the family Reoviridae and cause severe diarrhea in humans and animals (1). Rotaviruses are classified into 8 species (A to H) based on the genetic property of their inner capsid protein VP6 (2). The outer capsid proteins of rotaviruses (VP7 and VP4) are defined by the number of G and P genotypes, respectively, based on differences in gene sequence (1,3). Rotavirus A (RVA), rotavirus B (RVB), rotavirus C (RVC), and rotavirus H (RVH) are known to infect both humans and animals (1,2,4). While the epidemiology and protective immunity of RVA infection have been intensively studied (1,5), relatively little is known about non-A rotavirus infections.
Rotavirus Bs (RVBs) have been detected in humans and various animals, including cattle (1,6–8). Unlike RVA, RVB in humans primarily causes diarrhea in adults, as well as in children (9–11). In cattle, RVB has been associated with epidemic diarrhea in adults (12,13) and a marked decrease in milk production was observed in dairy cows in 1 study (14). Our serological surveys indicated the common occurrence of RVB infection in cattle (15). Triggers for epidemic outbreaks of RVB diarrhea remain unclear, however, as do circumstances that lead to subsequent RVB infection in adult cattle.
In the present study, we report on the epidemiological features of repeated outbreaks of epidemic diarrhea in adult cattle caused by RVB infection on a large dairy farm complex in Japan. Furthermore, we describe evidence of repeated RVB infection in the same cattle.
Materials and methods
Overview of farms
The large dairy farm complex was composed of 7 zones, with each zone consisting of 4 farm compartments (Figure 1). Each zone was 200 m apart and the compartments within the zones were 15 m apart. In 2002, 17 farms (Farms A to Q) had approximately 1400 adult cows (23 to 275/farm) and 200 growing cattle (0 to 60/farm). In 2005, 16 farms (Farm C had closed) had approximately 1500 adult cows (48 to 285/farm) and 320 growing cattle (7 to 46/farm). The same veterinarian provided medical care and artificial insemination at all farms, with the exception of farms A and F. Average renewal rates of adult milking cows per year were approximately 30% to 40%. Approximately 2/3 of replacement heifers were purchased from other dairies.
Figure 1.
Plan of large dairy farm complex in 2002 and in 2005, with capital letters indicating farm names. Farms with an outbreak of epidemic rotavirus B (RVB) diarrhea are shaded.
Clinical samples
During the first outbreak in 2002, fecal samples were collected from 20 diarrheal adult cows (aged over 24 mo) at the following affected farms: Farm E (n = 10), Farm D (n = 5), Farm J (n = 3), and Farm L (n = 2). During the second outbreak in 2005, fecal samples were collected from 28 diarrheal and 18 normal adult cows at the following affected farms: Farm E (n = 19), Farm D (n = 12), Farm L (n = 5), Farm Q (n = 5), and Farm G (n = 5). At least 2 or more diarrheal samples were collected at these farms. These feces were sampled within 4 d after the first finding of diarrhea at each farm. Serum samples were collected from these cows at the same time as fecal sampling at the acute phase and again 19 to 28 d later at the convalescent phase. During both outbreaks, overlapping sampling was conducted in 7 of these cows. Serum samples were also collected from adult cows 4 mo before the first outbreak in 2002 during a general health examination at the following farms: Farm E (n = 66), Farm D (n = 69), Farm A (n = 118), and Farm O (n = 71). Fecal samples were subjected to reverse transcription polymerase chain reaction (RT-PCR) and polyacrylamide gel electrophoresis (PAGE) of rotavirus double-stranded ribonucleic acid (dsRNA). Fecal samples were also tested for Salmonella species using a standard technique and Coccidium and Cryptosporidium species were checked by a sucrose flotation method.
RT-PCR
Viral RNA was extracted from fecal suspensions using TRIzol LS Reagent (Invitrogen, Carlsbad, California, USA) in accordance with the manufacturer’s instructions. Reverse transcription polymerase chain reaction (RT-PCR) assays were conducted using the OneStep RT-PCR Kit (QIAGEN, Valencia, California, USA) to detect the following genes: RVB (VP7 gene) (16), RVA (VP7 gene) (17), RVC (VP7 gene) (18), bovine torovirus (BToV) (N gene) (19), bovine coronavirus (BCV) (N gene) (20), and bovine viral diarrhea virus (BVDV) (5′ non-structural coding region) (21).
PAGE with viral dsRNA
Polyacrylamide gel electrophoresis (PAGE) of dsRNA extracted from diarrheal fecal samples was carried out with 7.5% precast gels (e-PAGEL; Atto, Tokyo, Japan) (22). The gels were stained with the Silver Stain Plus Kit (Bio-Rad, Hercules, California, USA) in accordance with the manufacturer’s instructions.
Virus antibody tests
Bovine RVB antibody was detected by enzyme-linked immunosorbent assay (ELISA) with recombinant baculovirus-expressed VP6 protein, as previously described (15). The RVB antibody titers were expressed as net optical density (OD), which was calculated as the OD from antigen-coated wells minus the OD from non-antigen-coated wells. A serum was considered RVB antibody-positive if net OD was greater than 0.2. Seroresponse was defined as an increase in net OD of 0.2 or more in paired sera. As previously described, virus neutralization tests were conducted for BVDV type 1 and bovine adenovirus type 3 (BAdV-3), using paired sera from affected and normal cows (23). Antibody titers against BCV and adenovirus type 7 (BAdV-7) were also determined by hemagglutination inhibition tests (24). Seroresponse was defined as a 4-fold or greater increase in paired serum antibody titers to the examined virus. Laboratory personnel were blinded to the disease status of the cattle when conducting the virus antibody tests.
Sequence analysis of the VP7 and VP4 genes of RVB
The full length VP7 gene of RVB from at least 2 fecal samples at each of 4 affected farms in 2002 and 5 affected farms in 2005 was produced by RT-PCR using the OneStep RT-PCR Kit (QIAGEN) with 5′ and 3′ end primers (13) and the PCR products were sequenced directly by cycle sequencing with an auto sequencer (ABI PRISM 3100; Life Technologies, Foster City, California, USA). The 5′-terminal region of the VP4 gene of RVB from 1 fecal sample per farm at 4 affected farms in 2002 and 3 affected farms in 2005 was amplified by RT-PCR with a pair of primers: 1F (5′-GGTATTTAATCACTAGGC-3′) and 1295R (5′-GGATTCAAACTGTTGTCAACTGG-3′). Reverse transcription polymerase chain reaction (RT-PCR) was carried out using the PrimeScript One Step RT-PCR Kit Version 2 (Takara, Shiga, Japan). The products were cloned into pCR2.1 TOPO vector (Life Technologies) and sequenced by cycle sequencing. Sequence data were aligned using the Clustal W method and phylogenetic trees were generated using the MegAlign program (Version 11.2.1) of Lasergene software (DNASTAR, Madison, Wisconsin, USA).
Statistical analysis
Seroprevalence of RVB among farms or cows was statistically analyzed by the Chi-square test or Fisher’s exact test using Ekuseru-Toukei 2012 (Social Survey Research Information, Tokyo, Japan).
Nucleotide sequence accession numbers
The newly determined sequences have been deposited in the DDBJ nucleotide (nt) sequence database and assigned the following accession numbers: D-2002 (VP7 gene, LC005523 and VP4 gene, LC005532); E-2002 (VP7 gene, LC005524 and VP4 gene, LC005533); J-2002 (VP7 gene, LC005525 and VP4 gene, LC005534); L-2002 (VP7 gene, LC005526 and VP4 gene, LC005535); D-2005 (VP7 gene, LC005527); E-2005 (VP7 gene, LC005528); G-2005 (VP7 gene, LC005529 and VP4 gene, LC005536); K-2005 (VP7 gene, LC005530 and VP4 gene, LC005537); and L-2005 (VP7 gene, LC005531 and VP4 gene, LC005538).
Results
Outbreaks of epidemic diarrhea in adult cows
In October 2002, epidemic diarrhea was first observed in some lactating adult cows at Farm G and then spread within 2 wk to approximately 550 out of 660 adult cows (83%) at 9 (Farms D, E, F, G, J, K, L, P, and Q) of 17 farms in a large dairy farm complex (Figure 1). Diarrhea spread through each farm within several days. Notably, 4 replacement heifers had been introduced at Farm G 2 d before the outbreak. Unfortunately, fecal samples had not been collected from these heifers because they did not show diarrhea at the time of outbreak.
In March 2005, another outbreak of epidemic diarrhea occurred in approximately 450 out of 700 adult cows (64%) at 9 (D, E, G, J, K, L, M, P, and Q) of 16 farms in the same complex (Figure 1). Diarrhea spread within several days at each individual farm and had affected these farms within 2 wk. No heifers had been newly introduced to any farms just before the outbreak. Eight of these 9 farms had also been hit by the previous outbreak in 2002.
Several common epidemiological features were observed between the outbreaks in 2002 and 2005. For example, affected cows had watery and brownish diarrhea, but not bloody diarrhea or fever, and each cow recovered 3 to 5 d after the onset of diarrhea without clinical treatment. Milk production decreased by an average of approximately 10%. During these outbreaks of adult cow diarrhea, no clinical signs, including diarrhea, were observed in the majority of growing cattle and calves. There were no significant differences between affected and non-affected farms in the mean number of adult cows in both outbreaks and in the mean annual renewal rates of milking cows from 2002 to 2005.
Fecal examination
Sixteen of 20 diarrheal fecal samples at 4 farms affected by the 2002 outbreak and 22 of the 28 diarrheal fecal samples at 5 farms affected by the 2005 outbreak were positive for RVB as determined by RT-PCR. In addition, 8 of 18 normal fecal samples collected at the same time as diarrheal samples at these affected farms in 2005 were also positive for RVB by RT-PCR. All diarrheal fecal samples were negative by RT-PCR for RVA, RVC, BCV, BoTV, and BVDV, however, and were also negative for Salmonella, Coccidium, and Cryptosporidium species.
PAGE with viral dsRNA
Of 14 fecal samples analyzed, 5 showed the characteristic migration patterns of dsRNA for RVB (pattern 4-2-2-3), based solely on PAGE analysis (Figure 2), and all were positive for RVB by RT-PCR. Notably, the migration pattern in 2002 was similar but not identical to that in 2005, with the spaces between RNA segments 5 and 6 and 7 and 8 in 2005 slightly wider than those in 2002 (Figure 2).
Figure 2.
Electrophoretic migration patterns of viral ribonucleic acids (RNAs) from feces positive for rotavirus B (RVB) by reverse transcription polymerase chain reaction (RT-PCR) in 2002 and 2005. Lanes indicate feces from each farm as follows: E (Farm E), D (Farm D), L (Farm L), K (Farm K), G (Farm G), and Q (Farm Q). E and D were collected in 2002 and L, K, G, and Q in 2005. The rotavirus A (RVA) lane indicates reference RVA strain OSU. Numbers and arrows indicate genome segments of rotaviruses. Characteristic migration patterns of double-stranded RNA (dsRNA) for RVB (pattern 4-2-2-3) were observed in lanes E, D, K, and G.
Virus antibody tests
Examination of paired sera from 20 affected cows from the outbreak in 2002 and 28 from 2005 showed no significant changes in antibody titers against BCV, BVDV type 1, BAdV-3, or BAdV-7. In contrast, a significant seroresponse (≥ 0.2 OD increase) to RVB was detected using ELISA in 16 of those 20 affected cows (80%) in 2002 and in 24 of the 28 cows (86%) in 2005 (Figures 3a and 3b). Taking into account these findings and the results of fecal examination, bovine RVB infection was considered to be the cause of both outbreaks of epidemic diarrhea. Interestingly, paired sera from 13 of 18 normal cows (72%) at the affected farms also exhibited a significant seroresponse to RVB (Figure 3c).
Figure 3.
Detection of rotavirus B (RVB) antibody by enzyme-linked immunosorbent assay (ELISA) with paired sera diluted 1:100 from adult cows with or without diarrhea in acute and convalescent phases during outbreaks of epidemic diarrhea in 2002 (a) and 2005 (b, c). Values above the dotted line [optical density (OD) = 0.2] indicate positive results for RVB antibody. Seroresponse was defined as an increase in OD of ≥ 0.2 in paired sera.
Inter- and intra-farm prevalence of RVB antibodies
Four months before the outbreak in 2002, RVB antibody-positive rates determined by ELISA in 135 adult cows at later affected Farms D and E were 32% and 30%, respectively. These rates were significantly lower than those determined by ELISA in 189 cows at later non-affected Farms A and O (67% and 61%, respectively; P < 0.01) (Table I). During the acute phase of the 2002 outbreak, the antibody-positive rate in 20 diarrheal cows at Farms D, E, J, and L was as low as 15% (Figure 3a). During the acute phase of the 2005 outbreak, the antibody-positive rate in 28 diarrheal cows (Farms D, E, G, L, and Q) was 26%, which was significantly lower than that in 18 non-diarrheal cows at 67% (Farms D and E) (P < 0.01) (Figures 3b and 3c).
Table I.
Prevalence of rotavirus B (RVB) antibody detected by enzyme-linked immunosorbent assay (ELISA) in sera of adult cows at farms 4 mo before an outbreak of epidemic RVB diarrhea in 2002
| Detection of RVB antibody | |||
|---|---|---|---|
|
|
|||
| Farm | Number positive | Sample number | (%) |
| Da | 21 | 66 | 31.8A |
| Ea | 21 | 69 | 30.4A |
| Ab | 79 | 118 | 66.9B |
| Ob | 43 | 71 | 60.6B |
Outbreak of epidemic RVB diarrhea occurred 4 mo later.
Outbreak of epidemic RVB diarrhea did not occur 4 mo later.
Values with different superscripts are significantly different (P < 0.01).
Responses to RVB in the same cattle
Four of 7 cows (57%) affected by RVB diarrhea in the 2002 outbreak exhibited RVB shedding in feces again in the 2005 outbreak, as determined by RT-PCR (Figure 4). Furthermore, 5 of these cows (71%) exhibited significant antibody-response with paired sera in the 2005 outbreak as determined by ELISA. It is notable, however, that none of these cows had diarrhea in the 2005 outbreak (Figure 4).
Figure 4.
Rotavirus B (RVB) antibody, incidence of diarrhea, and shedding of RVB in the same cows (n = 7) in 2002 and 2005. RVB antibody was detected by enzyme-linked immunosorbent assay (ELISA) with paired sera diluted 1:100 in acute and convalescent phases in outbreaks of epidemic diarrhea. Values above the dotted line [optical density (OD) = 0.2] indicate positive results for RVB antibody. Seroresponse was defined as an increase in OD of ≥ 0.2 in paired sera in each outbreak. Shedding of RVB was detected by reverse transcription polymerase chain reaction (RT-PCR) (1).
Sequence analysis of VP7 and VP4 genes of RVB
The nt sequences of VP7 genes of RVB from the same farms were identical at each outbreak. Therefore, VP7 gene sequences from 9 RVB strains (1 strain per farm in each outbreak) were indicated and designated as D-2002, E-2002, J-2002, L-2002, D-2005, E-2005, G-2005, K-2005, and L-2005. The VP7 gene sequences of these strains were 816 nts in length and most closely related to that of the bovine RVB Nemuro strain detected in Japan in 1997. When compared with the present strains, all VP7 genes examined were identical in the 2002 outbreak and similar to those in the 2005 outbreak. VP7 genes differed by 5 to 6 nts in the 2002 and 2005 strains, however, which reflected their distinct positions in the phylogenetic tree (Figure 5a).
Figure 5.
Phylogenetic trees for the VP7 gene (a) and the 5′-terminal region of VP4 gene (b) of bovine and human rotavirus B (RVB). The trees were generated using the MegAlign program of the Lasergene software (DNASTAR) on the basis of 772–816 bp of VP7 and 1265–1295 bp of VP4. The length of each pair of branches represents the distance between sequence pairs and the units at the bottom of the tree indicate the number of substitution events. Bootstrap values greater than 700 in 1000 pseudoreplicates are shown as percentages. The accession numbers of the nt sequences used for the tree construction are as follows: Nemuro, AB016818 (VP7 gene); MN10-1, JQ288103 (VP7 gene); ATI, U84472 (VP7 gene); WD653, U84141 (VP7 gene); Mebus, U84473 (VP7 gene); DB101, AY158155 (VP7 gene); DB180, AF529214 (VP7 gene); DB176, AF531910 (VP7 gene) and GQ358710 (VP4 gene); CAL, AF184083 (VP7 gene) and AF184084 (VP4 gene); Bang373, NC_021542 (VP7 gene) and NC_021543 (VP4 gene); WH-1, AY539856 (VP7 gene) and AY539857 (VP4 gene), ADRV, M33872 (VP7 gene) and M91434 (VP4 gene); IC-008, GU377216 (VP4 gene); and NIV-094456, JN009774 (VP4 gene). Bovine RVB strains from the present study are indicated by boldface type and their accession numbers are given in the text.
The 5′-terminal region of VP4 gene sequences from 7 RVB strains was determined and designated as D-2002, E-2002, J-2002, L-2002, G-2005, K-2005, and L-2005 and 1295 nt sequences of these strains were compared to those of published bovine and human RVB strains. Although the VP4 genes in viruses in the present study were found to be more closely related to those of bovine RVB strains detected in India (RUBV226, RUBV282, and DB176) than to human RVB strains, the nt sequence identities of the present and Indian bovine strains were relatively low (79% to 80%). When VP4 genes among the strains in the present study were compared, the strains were similar to each other, but as with the VP7 genes, the strains of 2002 were distinct from those of 2005 in the phylogenetic tree (Figure 5b).
Discussion
Viral diarrhea in adult cattle is caused by several viruses, including RVB (12–14). During the routine diagnosis of diarrhea in adult cattle, however, RVB infection is not typically considered due to the shortage of information about its clinical importance. Therefore, the epidemiology of RVB diarrhea in adult cattle still remains unclear. In this study, we observed that outbreaks of epidemic diarrhea with decreases in milk production caused by RVB infection in adult cows could occur repeatedly at the same farms just like epidemic diarrhea in adult cows caused by BCV infection (25). In addition, the epidemic diarrheas were observed mostly in adult cows, but not in growing cattle and calves, which is consistent with other reports (13,14).
In the present study, RVB antibody-positive rates at later affected farms were significantly lower than at later non-affected farms. In addition, the antibody-positive rates in affected cows were relatively low. In human RVA infections, the presence of serum antibody was a marker for protection against RVA infection and disease (26–28). Taken together, the outbreaks of epidemic RVB diarrhea in adult cows in this study might be associated with the antibody prevalence at each farm, i.e., herd immunity (29,30). Although the reasons for the observed inter-farm differences in prevalence of RVB antibody are unknown, RVB subclinical infection or sporadic diarrhea might have occurred at some farms with high seroprevalence. Notably, universal mass vaccination of children for human RVA has resulted in herd immunity, which reduces prevalence of RVA-associated disease even in older children who were not vaccinated (31).
The second outbreak in 2005 occurred at most of the farms that had been affected by the first outbreak in 2002. Although the reasons for this are not known, we consider that it does not contradict the theory of herd immunity for the following reason. On each farm of the complex, approximately 30% to 40% of milking cows were replaced annually and 2/3 of replacement heifers were purchased from outside. This means that, by 2004, almost half of milking cows might not have experienced the 2002 outbreak at all farms. Given the results of RVB VP7 and VP4 gene sequences, we consider it more likely that the strains spread among farms during each outbreak than that each strain persisted at each farm from the first outbreak and caused the second outbreak.
In humans, primary RVA infection does not usually lead to permanent immunity and reinfection can occur at any age (1,32), although subsequent infection is generally less severe (33,34). In addition, a cohort study of human RVA infection indicated that protection against homotypic reinfection appeared to last 2 y (35). In contrast, little information is available about immunity to RVB infection. The present study demonstrated that some adult cows became reinfected with RVB strains, in which VP4 and VP7 genes were closely related, at an interval of approximately 2 1/2 y. These cows did not exhibit diarrhea during the second outbreak, however, despite observations of RVB shedding. These results indicate that adult cows can be reinfected with RVB, but that subsequent infection might be less severe, which appears to be very similar to RVA infection. This information might help to control RVB diarrhea in humans and animals.
In conclusion, bovine RVB can repeatedly cause epidemic diarrhea with a decrease in milk production in adult cows at the same farms and the same adult cows can develop RVB infection repeatedly. A simple test to detect bovine RVB is being developed for further epidemiological investigation.
Acknowledgment
The authors thank Ms. Nachiko Hattori for her technical assistance.
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