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1 National Centre for Foreign Animal Disease, 1015 Arlington Street, Winnipeg MB, Canada
2 University of Manitoba, Department of Immunology, Basic Medical Sciences Building, 730 William Avenue, Winnipeg MB, Canada
3 CSIRO Livestock Industries, Australian Animal Health Laboratory, Private Bag 24, Geelong, Victoria 3220, Australia
4 Department of Animal Health of Vietnam, Regional Animal Health Centre, 124 Pham The Hien Street, District 8, Ho Chi Minh City, Vietnam
Correspondence
Shawn Babiuk
babiuks{at}inspection.gc.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are EU625262 and EU625263.
Supplementary tables are available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The geographical range of sheeppox and goatpox includes Africa, north of the Equator (Kitching et al., 1989), the Middle East, Turkey (O
uzolu et al., 2006), and Asia including India (Bhanuprakash et al., 2006) and China (Zheng et al., 2007). In contrast, the geographical range of lumpy skin disease (LSD) is restricted to Africa and includes South Africa, which itself is free of sheeppox and goatpox (Kitching et al., 1989). Currently capripoxviruses are expanding their distribution with recent LSDV outbreaks in Egypt and Israel (Yeruham et al., 1995), and outbreaks of goatpox in Greece, Mongolia and Vietnam (OIE World Animal Health Information Database). The Vietnam isolate came from a capripoxvirus outbreak when a farmer bought 120 goats from two provinces in the middle of Vietnam and added them to his herd of 200 Bach Thao goats. The outbreak occurred 2 weeks after the arrival of the new goats and was characterized by morbidity of around 60 % and a mortality rate of approximately 45 %. The origin of the Vietnam isolate was presumably China, through suspected illegal animal movements across the border.
Sheeppox and goatpox are severe acute diseases that have major impacts on small ruminant production in countries where disease is endemic, due to reduced milk yields, damage to hides and mortalities (Yeruham et al., 2007). The severity of clinical disease is variable depending on the host species, the breed and age of the susceptible host and the virus isolate (Kitching & Carn, 2004). Different isolates can behave differently in sheep and goats, with most isolates more virulent in either sheep or goats, while others are pathogenic in both species (Kitching et al., 1986). The nomenclature is largely made up of the location (country) and the species from where each virus isolate originated (sheep, goat or sheep and goat). This issue of naming strains SPPV, GTPV or sheep and goatpox virus remains problematic since historically the virus nomenclature has been based on field observation of the host species affected. There is little else to support the species strain designation except when the viruses are used to experimentally infect both hosts under controlled conditions. Given the large size of the viruses and the complexity of encoded factors likely to determine host specificity we have no other criteria upon which to base strain designation. LSDV, in contrast, appears to only cause clinical disease in cattle. Capripoxviruses are OIE immediately reportable diseases and are on the select agent list of the United States Department of Agriculture and the US National Select Agent Registry, since these viruses are considered potential bioterrorist agents.
There are no serotypes of capripoxvirus as SPPV, and GTPV and LSDV are antigenically indistinguishable (Kitching, 1986). DNA sequence analysis of capripoxvirus genomes revealed an identity of at least 96 % between SPPV, GTPV and LSDV and that these viruses are phylogenetically distinct (Tulman et al., 2001, 2002). Phylogenetic analysis of ORF 074, which is used in diagnostic tests for capripoxviruses (Heine et al., 1999), revealed not only that sheeppox, goatpox and LSD viruses clustered into distinct groups, but also the presence of likely species specific genetic signatures (Hosamani et al., 2004). However, additional and widespread genome information may be informative on this issue in the future.
The control of capripoxvirus disease in endemic countries is possible using a single live attenuated vaccine (Carn, 1993; Kitching et al., 1987; Kitching, 2003; Roth & Spickler, 2003). The use of live attenuated virus vaccines in disease-free countries is not an option, however, due to trade restrictions and the strategy for disease control by slaughter of infected animals. Currently, it is not possible to differentiate capripoxvirus-infected from vaccinated animals using serological tests (van Oirschot, 1999). Capripoxviruses can be used as vectors for other virus antigens such as rabies virus glycoproteins (Aspden et al., 2003), Rift Valley fever glycoproteins and nucleocapsid proteins (Wallace et al., 2006).
The purpose of this study was to improve the understanding of the pathogenesis of capripoxvirus infections in sheep and goats by infecting both species with Yemen or Vietnam virus isolates. Whereas the Yemen isolate had previously been shown to cause disease in both sheep and goats (Kitching et al., 1986), the Vietnam isolate was a previously uncharacterized virus, which had been isolated from goats during a recent outbreak in Vietnam, and its ability to cause disease in sheep was unknown.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and then twice in OA3.Ts cells at NCFAD (Babiuk et al., 2007). The Vietnam capripoxvirus isolate was originally obtained from an infected goat lung during the first passage on Vero cells at the Vietnam Regional Animal Health Centre (Department of Animal Health, Ho Chi Minh City, Vietnam). This virus was subsequently passaged twice in OA3.Ts cells at NCFAD.
Experimental infection.
Sheep and goats were experimentally infected by intradermal inoculation near the sixth rib with 0.2 ml non-plaque-purified virus (104.7 TCID50 of the Yemen isolate or 104.9 TCID50 of the Vietnam isolate). Rectal temperatures were recorded daily and animals inspected for clinical signs and the development of lesions at the inoculation site and elsewhere on the body. Comprehensive necropsies of one sheep and one goat were undertaken every second day from 4 days post-inoculation (p.i.) through to day 14 with six sheep undergoing necropsy following inoculation with either the Yemen or Vietnam isolate. The severity of disease in goats inoculated with the Yemen isolate necessitated the euthanasia of two goats each on days 9, 10 and 14 p.i., with no necropsy on days 12 p.i. The severity of disease in the goats inoculated with the Vietnam isolate also necessitated the euthanasia of one additional animal on day 14 p.i. for a total of seven necropsies with goats. Goats were provided with palliative care during the acute phase of disease including the administration of intravenous fluids to counter dehydration and antibiotics to control secondary bacterial infections. In sheep the disease was less severe following challenge with either the Yemen or Vietnam isolate allowing three sheep to survive until day 35 p.i., which enabled the collection of longer term samples from these animals. Animal experimentation was conducted under the approval of the Canadian Science Centre for Human and Animal Health Animal Care Committee, which follows the guidelines of the Canadian Council on Animal Care.
Sample collection.
Nasal, oral and conjunctival swabs, as well as blood samples, were collected on days –2, 4, 6, 8, 10, 12, 14, 18, 21, 28 and 35 p.i. Comprehensive necropsies of one sheep and one goat were undertaken every second day from 4 days p.i. through to day 14 with samples collected as described previously (Bowden et al., 2008) to prevent the risk of cross contamination between specimens.
DNA extraction from clinical samples.
DNA was extracted from blood or swabs using the QIAamp 96 DNA Blood kit (Qiagen) according to the manufacturer's instructions. For solid tissues, samples were processed in a Mini-BeadBeater-8 (Biospec Products), using two 25 s periods of homogenization separated by cooling on ice between cycles, to generate 10 % (w/v) homogenates in PBS (Sigma). DNA was extracted from the tissue homogenates using the DNeasy 96 Blood and Tissue kit (Qiagen) according to the manufacturer's instructions with an overnight proteinase K incubation at 56 °C.
Quantitative real-time PCR.
To determine viral genome copies in clinical samples a real-time PCR minor groove-binding (MGB) TaqMan assay that amplified and detected an 89 bp region within ORF 074 was used as described previously (Bowden et al., 2008), except that 5 µl purified DNA from each sample was used as template and reactions were run on an ABI Prism 7900 HT Sequence Detection System (Applied Biosystems).
Virus isolation from clinical samples.
Isolation of infectious virus from swabs, urine, blood (diluted 1 : 10 in PBS) (Sigma) and solid tissues [as 10 % (w/v) homogenates in PBS, prepared using a Mini-BeadBeater-8 (Biospec Products)] was performed by inoculation of samples onto 80–90 % confluent ovine testis cell monolayers (OA3.Ts; ATCC CRL-6546) grown in 12-well plates (ICN Biomedicals). Development of viral-induced cytopathic effect (CPE) on OA3.Ts cells was monitored for a period of 10 days following inoculation (Babiuk et al., 2007). Samples positive in 12-well plates were titrated in 96-well plates by 10-fold dilutions in quadruplicate and virus plaques were enumerated 6 days following inoculation.
Isolation and amplification of viral DNA.
DNA was extracted from 100 µl aliquots of Yemen and Vietnam GTPV stocks as described previously (Boyle et al., 2004), and dissolved in 50 µl 10 mM Tris, 1 mM EDTA, pH 8.0 (Sigma), containing 20 µg RNase (Sigma) ml–1. PCR primers were designed using Clone Manager (version 8, Scientific and Educational Software), synthesized by a commercial provider (Sigma Genosys) and used to generate overlapping products encompassing ORF 074. Reactions were conducted in duplicate using, as template, 2 µl 1 : 10 (v/v) dilution of viral DNA in water and the HotStarTaq Master Mix kit (Qiagen) following the recommendations of the manufacturer. Amplicons were purified using the QIAquick PCR Purification kit (Qiagen) and quantified by spectrophotometry (Nanodrop ND-1000; Thermo Scientific) prior to sequencing.
DNA sequencing and sequence analyses.
Both strands of duplicate PCR products were sequenced using dideoxy BigDye terminator chemistry (Applied Biosytems) and an Applied Biosystems 3130xl Genetic Analyzer (Applied Biosytems). Sequence assembly was performed using SeqMan (Lasergene version 7.2, DNASTAR), whilst pairwise alignments between ORF 074 of the Yemen or Vietnam isolate and that of other capripoxviruses were conducted using Clone Manager (version 9, Scientific and Educational Software).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The appetite and faecal output decreased dramatically in goats infected with either the Yemen or Vietnam isolate from 7 days p.i. to the end of the experiment. A few of the goats developed a noticeable purulent oculo-nasal discharge by 7 days p.i. The clinical signs observed in the goats included fever, mild increase in respiration, decreased appetite, decreased water consumption, decreased faeces production, depression, macules, papules, scabs, conjunctivitis and clear to yellow nasal discharge with crusting of the nares. Apart from the development of a small number of secondary skin lesions, sheep infected with the Vietnam isolate otherwise appeared clinically normal throughout the study period.
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). The nodules in the upper gastrointestinal tract and parenchymal organs appeared uniformly white throughout, raised and varied in size from pinpoint to 1 cm in diameter. In the lung there were multiple, red, raised, firm, round nodules with white centres that varied in size from pinpoint to 1 cm in diameter. All four compartments of the stomach contained both serosal and mucosal stellate white nodules. The omental fat contained numerous firm 1–3 cm thickened stellate nodules. The prescapular and inguinal lymph nodes were initially enlarged by 6 days p.i., and by 12 days p.i. a generalized lymphadenopathy had developed. The lymph nodes were enlarged up to five times the normal size, haemorrhagic and congested.
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and 3) followed by virus isolation (Supplementary Tables S1 and S2 available in JGV Online). The accumulation of viral DNA or infectious virions in nasal, conjunctival and oral secretions was first detected in goats infected with the Yemen or Vietnam isolate by 6 days p.i. At 8 days p.i., viral genomes were detected by real-time PCR in nasal, oral and conjunctival swabs from all of the goats infected with the Yemen isolate and the majority of the goats infected with the Vietnam isolate. Viral shedding continued in all goats infected with the Yemen isolate and the viral titres in these samples rose until euthanasia at 14 days p.i. In contrast, infectious virus was isolated in nasal, oral and conjunctival swabs from the majority of goats infected with the Vietnam isolate, for which the peak in the number of animals shedding occurred between days 10 and 14 and declined rapidly thereafter. Viral shedding continued to be detected in nasal, oral and conjunctival swabs from four of six samples from the surviving goats by real-time PCR until the conclusion of the study at 35 days p.i.
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Virus quantification in blood and solid tissues by virus isolation and real-time PCR
The kinetics of viraemia in capripoxvirus-infected sheep and goats were assessed initially using real-time PCR to detect viral genomes (Fig. 4) and subsequently by virus isolation in OA3.Ts cells to detect the presence of infectious virus. Viraemia was observed using real-time PCR as early as 6 days p.i. and lasted until 12 or 14 days p.i. in goats infected with the Vietnam or Yemen isolates, respectively. Virus was detected by virus isolation in the blood of several goats infected with the Yemen isolate between 8 and 10 days p.i. at low titres. Virus isolation was unable to detect virus in the blood of goats infected with the Vietnam isolate. Real-time PCR sporadically detected capripoxvirus in the blood of sheep infected with the Yemen isolate between 8 and 14 days p.i., and in only one sheep infected with the Vietnam isolate at 12 days p.i. Virus isolation detected virus sporadically in the blood of sheep infected with the Yemen isolate between 8 and 12 days p.i., but was unable to detect virus in the blood of sheep infected with the Vietnam isolate.
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and 3).
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Sheep and goat tissue homogenates were assessed by virus isolation on lamb testis cell monolayers and subsequently titrated to determine their infectivity. Virus was consistently isolated at high titres in skin from the inoculation site in both sheep and goats as well as in secondary skin lesions from goats (Tables 2
and 3). Virus was also isolated at high titres in lung, tongue and nasal mucosa from goats infected with either the Yemen or Vietnam isolate, although not consistently at every time point (Tables 2 and 3).
Genetic relationship between GTPV isolates
Pairwise alignments using ORF 074 (969 bp) of the Vietnam or Yemen virus isolate and that of other capripoxviruses revealed features within the primary sequence data that have previously been shown to be present in goatpox, but not sheeppox, virus isolates (Hosamani et al., 2004) (data not shown). Furthermore, the sequence derived from ORF 074 of the Vietnam, but not the Yemen, isolate was 100 % identical to that of several GTPV isolates from China (GenBank accession nos AY773088
[GenBank]
, EF514890
[GenBank]
and EF522176
[GenBank]
), which is consistent with the Vietnam isolate having originated in that country.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). A more natural challenge by infection of mucosal surfaces such as intranasal administration or contact infection experiments, where infected animals are housed with uninfected animals, might better reflect the pathogenicity of each isolate. However, these are not easy experiments to perform due to the difficulty in synchronizing the infection of each animal, which is critical to studying the spread of the virus in vivo. Virulent isolates of SPPV have been evaluated by both intradermal as well as intranasal routes of infection and both caused similar disease (Balinsky et al., 2007; Kitching & Taylor, 1985b).
The high titres of virus in the skin of capripoxvirus-infected animals suggest the possibility that SPPV and GTPV can be transmitted by biting insects as vectors. Stomoxys calcitrans is capable of transmitting sheeppox and goatpox mechanically under experimental conditions (Mellor et al., 1987) and Aedes aegypti has been shown to be involved in LSDV transmission (Chihota et al., 2001). Although insect vectors are not necessary for the transmission of sheeppox and goatpox, they could be responsible for longer distance transmission.
This study revealed the spread of each challenge virus from the inoculation site to multiple organs, predominantly skin and to a lesser extent lung, prior to detectable viraemia. The viraemia possibly originated from macrophages infected from virus produced in the skin (Gulbahar et al., 2006). Viraemia was observed for a short period starting at 6 days p.i. and lasting until 14 days p.i., at which time the host-immune response had eliminated most of the virus circulating in the blood. Viraemia was not detectable in all animals by virus isolation. Although virus was isolated from several lymph nodes, the titres were lower and not consistently observed throughout the sampling period compared with skin lesions. The involvement of the viscera was largely limited to discrete lesions of limited number appearing late in the course of the disease.
There were isolate-specific differences in terms of early detection in swabs from different anatomical sites by real-time PCR. Nasal, oral and conjunctival swabs from goats infected with the Yemen isolate were positive by 6 days p.i., whereas nasal and oral swabs were positive by 6 days p.i. and conjunctival swabs by 8 days p.i. in sheep infected with the Yemen isolate as well as goats infected with the Vietnam isolate. Sheep infected with the Vietnam isolate displayed limited shedding in nasal and oral swabs detected by real-time PCR. These results differ from another study where SPPV DNA was detected by real-time PCR in nasal swabs as early as 2 days p.i. (Balinsky et al., 2008), probably because these sheep were inoculated intranasally. These results illustrate that different capripoxvirus isolates can have different kinetics of viral shedding depending on the isolate, species and route of viral inoculation.
SPPV and GTPV replicate in multiple organs with skin being the most permissive followed by discrete sites within oronasal tissues and gastrointestinal tract, as well as lung (Bowden et al., 2008). The quantity of infectious virus shed in goats infected with the Yemen isolate was high until death. Detection of capripoxvirus DNA by real-time PCR in mucosal swabs continued well after the virus was undetectable in the blood and persisted up to 28 days p.i. in sheep infected with the Yemen isolate and up to 35 days p.i. in goats infected with the Vietnam isolate. It is likely that surviving goats infected with the Yemen isolate would behave similarly. The ability to detect capripoxvirus in nasal, oral and conjunctival swabs allows for easier surveillance and disease confirmation compared with skin biopsies. However, the duration of viral shedding may vary considerably depending on the isolate, with the presence of infectious virus in mucosal secretions of some sheep following experimental infection with an SPPV isolate from Nigeria having been observed for up to 2 months following the onset of clinical disease (Bowden et al., 2008).
The results of this study support the view that most strains of SPPV or GTPV have a host preference for either sheep or goats, since following experimental infection with either the Vietnam or Yemen isolate, goats developed more severe disease than sheep. This is in agreement with previous studies demonstrating that different isolates of SPPV or GTPV can transfer between sheep and goats, causing severe clinical disease in one species and less severe disease in the other (Kitching & Carn, 2004). Although previous studies considered the Yemen isolate equally pathogenic in Soay sheep and British white goats (Kitching et al., 1986), these contrasting findings are most likely due to differences in breed and age of the sheep used.
The level of virus infection as determined by virus isolation and real-time PCR was much higher in goats infected with the Yemen and Vietnam isolates than in sheep and appeared to correlate with the severity of disease observed in each species. It is currently unknown which viral genes are responsible for determining host specificity. It would be possible to identify genes responsible for virulence through sequencing and comparing different capripoxviruses that have been characterized for virulence in sheep and goats. The function of these genes could then be confirmed by the generation of recombinant capripoxviruses similar to what was done to characterize the role of a kelch-like gene in virulence (Balinsky et al., 2007). It is likely that only a small number of amino acid changes in a few genes may be involved in species specificity (Kara et al., 2003). The host specificity is probably linked to the dissemination and growth of the virus in sheep and goats in vivo, as the Vietnam isolate grows equally as well as SPPV in lamb testis cells (data not shown).
Although both capripoxviruses demonstrate a distinct host preference for goats compared with sheep, the Yemen isolate appears to be more pathogenic in general. It would appear from sequencing of ORF 074 that both isolates have the ‘signature’ typical of other goat-adapted capripoxviruses (Hosamani et al., 2004). In addition, the sequence derived from ORF 074 of the Vietnam isolate was identical to that of several GTPV isolates from China, which is consistent with the Vietnam isolate being of Chinese origin. The entry of goatpox into Vietnam is a concern and illustrates the potential of capripoxviruses to spread to previously uninfected countries. Countries surrounding capripoxvirus-infected areas should be prepared to respond to potential outbreaks.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 4 June 2008;
accepted 26 August 2008.
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