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Research ArticleGenetic Diversity of Bovine Viral Diarrhea Virus Infection inGoats in Southwestern China
Yu Deng 1 SiluWang1 Runxia Liu2 and Guiying Hao1
1School of Animal Science Xichang College Xichang 615013 China2South Dakota State University Brookings SD 57007 USA
Correspondence should be addressed to Yu Deng dengyu127gmailcom
Received 9 August 2018 Accepted 11 October 2018 Published 18 November 2018
Academic Editor William Alberto Canon-Franco
Copyright copy 2018 Yu Deng et alThis is an open access article distributed under the Creative Commons Attribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
Bovine viral diarrhea virus (BVDV) affects cows pigs sheep goats and other ruminants as well as some wild animals BVDVcauses considerable economic losses every year and many countries have developed programs aimed at the eradication of thisdisease The genetic diversity of BVDV in diseased goats has never been described in southwestern China Thus in this study weapplied antigen-capture ELISA and RT-PCR to survey the infection rate of BVDV in diseased goats in this region Our resultsdemonstrated that the average BVDV infection rate in goats was 1751 with all positive samples indicating infection by BVDV-1 and not BVDV-2 BVDV-3 or Border disease virus The molecular characteristics of the 51015840-untranslated region (51015840-UTR) ofBVDV-1 were recognized as belonging predominantly to the BVDV-1a 1b 1c 1m and 1p subtypes BVDV-1b and 1m were the mostabundant subtypes identified in this region similar to the BVDV epidemics in cattle in other regions of ChinaThis is the first studythat describes the genetic characterization of BVDV in sick goats from southwestern China and is important for future studies andcontrol programs
1 Introduction
Bovine viral diarrhea virusndash1 (BVDVndash1) and BVDVndash2together with classical swine fever virus and border diseasevirus (BDV) are currently classified as the genus Pestivirusand family Flaviviridae [1] A new unclassified Pestivirusspecies HoBi-like virus was first identified in fetal bovineserum from Brazil and was related to BVDV at the antigenicand genetic levels Thus the viruses were referred to asldquoBVDVndash3rdquo [2] To date a growing number unassignedatypical Pestivirus species have been detected in EuropeNorth America South America and Asia [3] however suchemerging pestiviruses have not been officially recognized Toresolve the taxonomy of pestiviruses a new taxonomy for thegenus Pestivirus (family Flaviviridae)was proposed where allspecies were redesignated as Pestivirus A-Pestivirus K [4]
The natural host of BVDV is cattle though it is alsocapable of infecting sheep goats piglets and other domesticand wild ruminants by persistently infected (PI) animalsand transiently infected individuals [5] PI cattle are themain source of BVDV however persistent infections alsooccur in nonbovid hosts such as sheep and deer BVDV
infections in goats typically result in reproductive diseasesand viable PI goats are rare [6] There is increasing evidencethat BVDV infections occur in a wider range of speciesincluding mountain goats and domestic goats that have beenreservoirs for BVDV infection and seriously impact thedomestic livestock industry
BVDV has a single stranded positive sense RNA genomeof 123ndash125 kbThe full-length viral genome is flanked at bothends by 51015840 and 31015840 untranslated regions (UTRs) and contains asingle open reading frame that encodes a single polyproteinthat is approximately 4000 amino acidsThe genetic diversityof novel Pestivirus strains is usually based on the characteris-tics of partial sequences from the 51015840ndashUTR Npro or E2 regionsof the genome However the 51015840ndashUTR of Pestiviruses hasthe highest degree of sequence conservation and is thereforemost frequently used for phylogenetic analysis Accordingto sequence comparison analyses of this region there are21 subtypes of BVDVndash1(1andash1u) [7ndash9] and four subtypes ofBVDVndash2 (2andash2d) [10ndash12]
A previous study based on a strain of BVDVndash1 thatinfected goats in easternChina showed that a high proportion
HindawiJournal of Veterinary MedicineVolume 2018 Article ID 8274397 5 pageshttpsdoiorg10115520188274397
2 Journal of Veterinary Medicine
Table 1 Description of the 12 isolates used in this study
Name of thepositivesamples
Year SymptomsRegion of the
samplescollected
GenBankAccessionnumber
subtype Identity ()1a
NADL1b
Osloss1c
Mannasi1m
ZM951p
TJ06
DF1312 2013 Respiratorysymptom DF MG323517 1m 954
DC1301 2013 Diarrhea DC MG323518 1b 980DS1324 2013 Weak DS MG323520 1a 879MN1319 2013 Diarrhea MN MG323522 1b 980CF1374 2013 Diarrhea CF MG323527 1m 957HL1407 2014 Abortion HL MG323523 1b 916FS1426 2014 Weak FS MG323525 1p 984XC1522 2015 Mucosal disease XC MG323516 1b 970DB1503 2015 Abortion DB MG323519 1m 970
FS1573 2015 Respiratorysymptom FS MG323524 1c 975
FS1605 2016 Respiratorysymptom FS MG323521 1m 957
SC1601 2016 Respiratorysymptom SC MG323526 1b 970
(29236) of BVDVndashpositive goats came from eastern China[13] However studies regarding the genetic diversity ofBVDV in diseased goats in southwestern China remain rareThus this study detected and genotyped BVDV from infectedgoats in this region
2 Materials and Methods
21 Samples A total of 217 blood samples taken from dis-eased goats that presented with symptoms such as diarrhearespiratory tract infection and mucositis were collectedbetweenMarch 2013 and April 2016 frommultiple goat farmsin southwestern China
22 BVDV Antigen-Capture ELISA (ACE) Sera werescreened for BVDV using IDEXX BVD Ag Test (IDEXXlaboratories Inc Shanghai China) which can be appliedfor detection of genetically diverse BVDV strains accordingto the manufacturerrsquos instructions The antigen-positivesamples were then followed up with RT-PCR detection
23 RNA Isolation and RT-PCR Detection of BVDVndash1BVDVndash2 BVDVndash3 and BDV Viral RNAwas extracted from200 120583L aliquots of goat serum using the QIAamp Viral RNAMini Kit (QIAGEN China Shanghai China) following themanufacturerrsquos recommendations Four different PCR assaysfor BVDVndash1 [14] BVDVndash2 [15] BVDVndash3 [16] and BDV [17]were performed to amplify the respective targets The PCRproducts were purified and sequenced by the JIELI BiologyCompany (Shanghai China)
24 Phylogenetic Analysis The 51015840ndashUTR genomic sequencesobtained were compared with the relevant sequences pub-lished in GenBank (httpwwwncbinlmnihgovgenbank)using the Basic Local Alignment Search Tool (BLAST) The
sequences in this study were trimmed and analyzed withMEGA70 software [18] to obtain 224 nucleotide sequencescorresponding to the 51015840ndashUTR region of BVDV The 224nucleotide sequences were then subjected to alignment usingthe ClustalW program using MegAlign in the Lasergene120 software (DNASTAR Inc Madison WI USA) andgenetic diversity analysis was performed using MEGA70software The evolutionary distances in the phylogenetic treewere computed using the Tamura 3ndashparameter model with1000 bootstrap replicates each constructed by the Neighbor-Joining method [18]
3 Results
The results of ACE showed that out of the 217 diseased goatsera samples tested using ACE 30 were antigen-positive forBVDV Antigen-positive samples were confirmed as BVDV-1 using BVDV-1 specific nested RT-PCR Fifteen additionalsamples that were close to the cutoff value of ACE were alsotested with nested RT-PCR eight of which were positive forBVDV-1 Taken together 38 sequences from 217 total samplescorresponded to BVDVndash1 by nested RT-PCR which resultedin a 197ndashbp amplicon from the BVDVndash1 51015840ndashUTR HoweverBVDVndash2 BVDVndash3 and BDV were not detected in any ofthese samples using RT-PCRThese results indicated that theaverage infection rate of BVDVndash1 in goats was 1751 (38217)in southwestern China
BVDVndash1was detected in 12 of 38BVDVndashpositive samplesby first roundRT-PCR which produced a 305 bp product thatwas not detected in the other 26 BVDVndash1ndashpositive samplesThe sequences detected with the first round RT-PCR in the 12BVDVndash1 positive samples were deposited in GenBank underaccession numbers MG323516ndashMG323527 (Table 1)
Twelve of those sequences were selected for the construc-tion of a phylogenetic tree and were divided into five differentsubtypes Five isolates (XC1522 HL1407DC1301 SC1601 and
Journal of Veterinary Medicine 3
Figure 1 Phylogenetic tree of a 224 bp portion of the 51015840-UTR nucleotide sequences The BVDV strains isolated from goats in southwesternChina with Pestivirus reference strains of BVDV-1 BVDV-2 BVDV-3 and BDV registered in GenBank database The tree was constructedusing the Neighbor-Joining method bootstrapping (1000 replications) and the Kimura three parameter statistical model of MEGA 70software The 12 isolated sequences from goat serum in this study are designated with ldquoblue circlerdquo
MN1319) were clustered within BVDVndash1b one (DS1324) wastyped as BVDVndash1a one (FS1573) as BVDVndash1c one (FS1426)as BVDVndash1p and four (FS1605 CF1374 DF1312 andDB1503)were characterized as BVDVndash1m No BVDVndash2 BVDVndash3 orBDV was detected in field isolates by phylogenetic analysis
4 Discussion
In this study we identified 12 selected BVDV-1-positivesamples that represented different flocks or geographicalorigins of blood samples collected between 2013 and 2016
Experimental or natural infection in goats has been previ-ously confirmed [19] Goats infected with BVDV representa great risk for disease transmission thus making the identi-fication of BVDV infection in goats an important endeavorThis investigation described the genetic diversity of BVDVisolated from goats in southwestern China and demonstratedthe occurrence of at least five subtypes of BVDV includingBVDVndash1a 1b 1c 1m and 1p
Among the BVDVndash1 types the most frequent subtypewas BVDVndash1b (n=5) (Table 1 and Figure 1) Five BVDVndash1b-positive samples from different counties of southwestern
4 Journal of Veterinary Medicine
China shared 981ndash990 identity with each other and had916ndash980 identity with the reference strain BVDVndash1b24ndash15 (AF298060) and Osloss (M96687) Those five strainswere also clustered with the two BVDV-1b reference strains(Figure 1) In cattle BVDVndash1b was first detected in thetissue of a bovine fetus in 1980 in China and continu-ally isolated and identified in Tianjin Hebei Gansu Xin-jiang and Heilongjiang province from then onward [8 2021]
The 1b subtype is widely considered to be a majorcontributor to infection in Chinese cattle [20 22] SimilarlyBVDV-1b is also a main subtype in Chinese goat herds[13] BVDV transmission among different animal species hasbeen proven and therefore increased surveillance of BVDVinfection in goats should be an important factor to considerin the control and understanding of BVDV infection incattle
BVDVndash1m is another major subtype in this region (Fig-ure 1) Four BVDV-1-positive samples identified in this studywere classified as BVDVndash1m The isolates FS1605 CF1374DF1312 and DB1503 had 945ndash987 homology with eachother and shared 954ndash970homologywith theBVDVndash1mreference strain ZMndash95 (AF526381) (Table 1) Thereforethose four positive samples were clustered into BVDVndash1mBVDVndash1m was first isolated from a diseased pig in 1995 inChina [23] According to a survey conducted between 2005and 2013 this subtype has been widely distributed in Chinaand is the most prevalent among BVDVndash1 subtypes [12]
Our positive samples DS1324 FS1573 and FS1426respectively shared 879 975 and 984 sequence iden-tity with the reference strains BVDVndash1a NADL (M31182)BVDVndash1c Manasi (EU159702) Bega (AF049221) BVDVndash1pTJ06 (GU120246) and TJ07 (GU120247) (Table 1) Thesepositive samples were classified into BVDVndash1a 1c and 1pwhich are not commonly found
In summary this study demonstrated that BVDVndash1was a common causative agent for infection of goats insouthwestern China and that 1751 of the detected samplesfrom ill goats were BVDVndash1 positive However we did notassess samples from the healthy goats and cannot determinethe prevalence of BVDV in healthy goats To further ourunderstanding of the genetic diversity of BVDV strainsdetected all antigen-positive samples were confirmed andcharacterizedwith RT-PCR as being infected by BVDVndash1 butnot BVDVndash2 BVDVndash3 or BDV Twelve BVDVndash1-positivesamples were identified from these RT-PCR positive samplesand were clustered into the six subtypes BVDVndash1a 1b 1c 1mand 1p Due to the possibility of cross infections of BVDVthat might occur among cattle piglets and goats muchmore emphasis should be placed on epidemiology surveysin these animals This is the first description of the geneticdiversity of BVDVndash1-positive samples collected from goats insouthwestern China
Data Availability
The data used to support the findings of this study areincluded within the article
Ethical Approval
No studies involving human participants or animals per-formed by any of authors are described in this article
Conflicts of Interest
The authors declare that there are no conflicts of interest inthis study
Authorsrsquo Contributions
Yu Deng and Guiying Hao designed and performed theexperiments Silu Wang contributed to the clinical diagnosisand collected samples YuDeng and Runxia Liu analyzed dataand wrote the manuscript All authors read and approved thefinal manuscript
Acknowledgments
This study was supported by the Applied FoundationProject of the Sichuan Provincial Science and TechnologyDepartment (2018JY0243) the Key Foundation Project ofthe Sichuan Provincial Education Department (18ZD0442)the ldquoDouble high talentrdquo Project of Xichang College(LGZ201712) and the postdoctoral scholarship of ChinaScholarship council (CSC201408515154)
References
[1] L Liu H Xia NWahlberg S Belak and C Baule ldquoPhylogenyclassification and evolutionary insights into pestivirusesrdquoVirol-ogy vol 385 no 2 pp 351ndash357 2009
[2] F V Bauermann J F Ridpath R Weiblen and E F FloresldquoHoBi-like viruses An emerging group of pestivirusesrdquo Journalof Veterinary Diagnostic Investigation vol 25 no 1 pp 6ndash152013
[3] J F Ridpath ldquoEmerging pestiviruses infecting domestic andwildlife hostsrdquo Animal Health Research Reviews vol 16 no 1pp 55ndash59 2015
[4] D B Smith G Meyers J Bukh et al ldquoProposed revision to thetaxonomy of the genus Pestivirus family Flaviviridaerdquo Journalof General Virology vol 98 no 8 pp 2106ndash2112 2017
[5] J F Ridpath ldquoBovine viral diarrhea virus global statusrdquoVeterinary Clinics of North America Food Animal Practice vol26 no 1 pp 105ndash121 2010
[6] T Passler K P Riddell M A Edmondson et al ldquoExperimentalinfection of pregnant goats with bovine viral diarrhea virus(BVDV) 1 or 2rdquo Veterinary Research vol 45 no 1 p 38 2014
[7] Y Abe T Tamura S Torii et al ldquoGenetic and antigeniccharacterization of bovine viral diarrhea viruses isolated fromcattle inHokkaido Japanrdquo Journal of VeterinaryMedical Sciencevol 78 no 1 pp 61ndash70 2016
[8] MDeng S JiW Fei et al ldquoPrevalence study and genetic typingof Bovine Viral Diarrhea Virus (BVDV) in four bovine speciesin Chinardquo PLoS ONE vol 10 no 4 2015
[9] S Silveira M N Weber A C S Mosena et al ldquoGeneticdiversity of brazilian bovine pestiviruses detected between 1995and 2014rdquo Transboundary and Emerging Diseases vol 64 no 2pp 613ndash623 2017
Journal of Veterinary Medicine 5
[10] L Elvira Partida M Fern Ndez J Guti Rrez et al ldquoDetectionof Bovine Viral Diarrhoea Virus 2 as the Cause of AbortionOutbreaks on Commercial Sheep Flocksrdquo Transboundary andEmerging Diseases vol 64 pp 19ndash26 2017
[11] M JenckelD HoperH Schirrmeier et al ldquoMixed triple Alliedviruses in unique recent isolates of highly virulent type 2 bovineviral diarrhea virus detected by deep sequencingrdquo Journal ofVirology vol 88 no 12 pp 6983ndash6992 2014
[12] K Yesilbag G Alpay and P Becher ldquoVariability and globaldistribution of subgenotypes of bovine viral diarrhea virusrdquoViruses vol 9 p 128 2017
[13] L Mao W Li L Yang et al ldquoPrimary surveys on molecularepidemiology of bovine viral diarrhea virus 1 infecting goats inJiangsu province Chinardquo BMC Veterinary Research vol 12 p181 2016
[14] Y Deng C-Q Sun S-J Cao et al ldquoHigh prevalence ofbovine viral diarrhea virus 1 in Chinese swine herdsrdquoVeterinaryMicrobiology vol 159 no 3-4 pp 490ndash493 2012
[15] M N Weber S Silveira G Machado et al ldquoHigh frequencyof bovine viral diarrhea virus type 2 in Southern Brazilrdquo VirusResearch vol 191 no 1 pp 117ndash124 2014
[16] V Mari M Losurdo M S Lucente et al ldquoMultiplex real-timeRT-PCR assay for bovine viral diarrhea virus type 1 type 2 andHoBi-like pestivirusrdquo Journal of Virological Methods vol 229pp 1ndash7 2016
[17] H Albayrak S O Gumusova E Ozan and Z Yazici ldquoMolecu-lar detection of pestiviruses in aborted foetuses from provincesin northern Turkeyrdquo Tropical Animal Health and Productionvol 44 no 4 pp 677ndash680 2012
[18] S Kumar G Stecher and K Tamura ldquoMEGA7 MolecularEvolutionary Genetics Analysis version 70 for bigger datasetsrdquoMolecular Biology and Evolution vol 33 no 7 pp 1870ndash18742016
[19] D D Nelson M J Dark D S Bradway et al ldquoEvidence forpersistent Bovine viral diarrhea virus infection in a captivemountain goat (Oreamnos americanus)rdquo Journal of VeterinaryDiagnostic Investigation vol 20 no 6 pp 752ndash759 2008
[20] F Xue Y-M Zhu J Li et al ldquoGenotyping of bovine viraldiarrhea viruses from cattle in China between 2005 and 2008rdquoVeterinary Microbiology vol 143 pp 379ndash383 2010
[21] F Zhong N Li X Huang et al ldquoGenetic typing and epidemi-ologic observation of bovine viral diarrhea virus in WesternChinardquo Virus Genes vol 42 no 2 pp 204ndash207 2011
[22] S Gao J Luo J Du et al ldquoSerological and molecular evi-dence for natural infection of Bactrian camels with multiplesubgenotypes of bovine viral diarrhea virus in Western ChinardquoVeterinary Microbiology vol 163 no 1-2 pp 172ndash176 2013
[23] X Xu Q Zhang X Yu et al ldquoSequencing and comparativeanalysis of a pig bovine viral diarrhea virus genomerdquo VirusResearch vol 122 no 1-2 pp 164ndash170 2006
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Submit your manuscripts atwwwhindawicom
2 Journal of Veterinary Medicine
Table 1 Description of the 12 isolates used in this study
Name of thepositivesamples
Year SymptomsRegion of the
samplescollected
GenBankAccessionnumber
subtype Identity ()1a
NADL1b
Osloss1c
Mannasi1m
ZM951p
TJ06
DF1312 2013 Respiratorysymptom DF MG323517 1m 954
DC1301 2013 Diarrhea DC MG323518 1b 980DS1324 2013 Weak DS MG323520 1a 879MN1319 2013 Diarrhea MN MG323522 1b 980CF1374 2013 Diarrhea CF MG323527 1m 957HL1407 2014 Abortion HL MG323523 1b 916FS1426 2014 Weak FS MG323525 1p 984XC1522 2015 Mucosal disease XC MG323516 1b 970DB1503 2015 Abortion DB MG323519 1m 970
FS1573 2015 Respiratorysymptom FS MG323524 1c 975
FS1605 2016 Respiratorysymptom FS MG323521 1m 957
SC1601 2016 Respiratorysymptom SC MG323526 1b 970
(29236) of BVDVndashpositive goats came from eastern China[13] However studies regarding the genetic diversity ofBVDV in diseased goats in southwestern China remain rareThus this study detected and genotyped BVDV from infectedgoats in this region
2 Materials and Methods
21 Samples A total of 217 blood samples taken from dis-eased goats that presented with symptoms such as diarrhearespiratory tract infection and mucositis were collectedbetweenMarch 2013 and April 2016 frommultiple goat farmsin southwestern China
22 BVDV Antigen-Capture ELISA (ACE) Sera werescreened for BVDV using IDEXX BVD Ag Test (IDEXXlaboratories Inc Shanghai China) which can be appliedfor detection of genetically diverse BVDV strains accordingto the manufacturerrsquos instructions The antigen-positivesamples were then followed up with RT-PCR detection
23 RNA Isolation and RT-PCR Detection of BVDVndash1BVDVndash2 BVDVndash3 and BDV Viral RNAwas extracted from200 120583L aliquots of goat serum using the QIAamp Viral RNAMini Kit (QIAGEN China Shanghai China) following themanufacturerrsquos recommendations Four different PCR assaysfor BVDVndash1 [14] BVDVndash2 [15] BVDVndash3 [16] and BDV [17]were performed to amplify the respective targets The PCRproducts were purified and sequenced by the JIELI BiologyCompany (Shanghai China)
24 Phylogenetic Analysis The 51015840ndashUTR genomic sequencesobtained were compared with the relevant sequences pub-lished in GenBank (httpwwwncbinlmnihgovgenbank)using the Basic Local Alignment Search Tool (BLAST) The
sequences in this study were trimmed and analyzed withMEGA70 software [18] to obtain 224 nucleotide sequencescorresponding to the 51015840ndashUTR region of BVDV The 224nucleotide sequences were then subjected to alignment usingthe ClustalW program using MegAlign in the Lasergene120 software (DNASTAR Inc Madison WI USA) andgenetic diversity analysis was performed using MEGA70software The evolutionary distances in the phylogenetic treewere computed using the Tamura 3ndashparameter model with1000 bootstrap replicates each constructed by the Neighbor-Joining method [18]
3 Results
The results of ACE showed that out of the 217 diseased goatsera samples tested using ACE 30 were antigen-positive forBVDV Antigen-positive samples were confirmed as BVDV-1 using BVDV-1 specific nested RT-PCR Fifteen additionalsamples that were close to the cutoff value of ACE were alsotested with nested RT-PCR eight of which were positive forBVDV-1 Taken together 38 sequences from 217 total samplescorresponded to BVDVndash1 by nested RT-PCR which resultedin a 197ndashbp amplicon from the BVDVndash1 51015840ndashUTR HoweverBVDVndash2 BVDVndash3 and BDV were not detected in any ofthese samples using RT-PCRThese results indicated that theaverage infection rate of BVDVndash1 in goats was 1751 (38217)in southwestern China
BVDVndash1was detected in 12 of 38BVDVndashpositive samplesby first roundRT-PCR which produced a 305 bp product thatwas not detected in the other 26 BVDVndash1ndashpositive samplesThe sequences detected with the first round RT-PCR in the 12BVDVndash1 positive samples were deposited in GenBank underaccession numbers MG323516ndashMG323527 (Table 1)
Twelve of those sequences were selected for the construc-tion of a phylogenetic tree and were divided into five differentsubtypes Five isolates (XC1522 HL1407DC1301 SC1601 and
Journal of Veterinary Medicine 3
Figure 1 Phylogenetic tree of a 224 bp portion of the 51015840-UTR nucleotide sequences The BVDV strains isolated from goats in southwesternChina with Pestivirus reference strains of BVDV-1 BVDV-2 BVDV-3 and BDV registered in GenBank database The tree was constructedusing the Neighbor-Joining method bootstrapping (1000 replications) and the Kimura three parameter statistical model of MEGA 70software The 12 isolated sequences from goat serum in this study are designated with ldquoblue circlerdquo
MN1319) were clustered within BVDVndash1b one (DS1324) wastyped as BVDVndash1a one (FS1573) as BVDVndash1c one (FS1426)as BVDVndash1p and four (FS1605 CF1374 DF1312 andDB1503)were characterized as BVDVndash1m No BVDVndash2 BVDVndash3 orBDV was detected in field isolates by phylogenetic analysis
4 Discussion
In this study we identified 12 selected BVDV-1-positivesamples that represented different flocks or geographicalorigins of blood samples collected between 2013 and 2016
Experimental or natural infection in goats has been previ-ously confirmed [19] Goats infected with BVDV representa great risk for disease transmission thus making the identi-fication of BVDV infection in goats an important endeavorThis investigation described the genetic diversity of BVDVisolated from goats in southwestern China and demonstratedthe occurrence of at least five subtypes of BVDV includingBVDVndash1a 1b 1c 1m and 1p
Among the BVDVndash1 types the most frequent subtypewas BVDVndash1b (n=5) (Table 1 and Figure 1) Five BVDVndash1b-positive samples from different counties of southwestern
4 Journal of Veterinary Medicine
China shared 981ndash990 identity with each other and had916ndash980 identity with the reference strain BVDVndash1b24ndash15 (AF298060) and Osloss (M96687) Those five strainswere also clustered with the two BVDV-1b reference strains(Figure 1) In cattle BVDVndash1b was first detected in thetissue of a bovine fetus in 1980 in China and continu-ally isolated and identified in Tianjin Hebei Gansu Xin-jiang and Heilongjiang province from then onward [8 2021]
The 1b subtype is widely considered to be a majorcontributor to infection in Chinese cattle [20 22] SimilarlyBVDV-1b is also a main subtype in Chinese goat herds[13] BVDV transmission among different animal species hasbeen proven and therefore increased surveillance of BVDVinfection in goats should be an important factor to considerin the control and understanding of BVDV infection incattle
BVDVndash1m is another major subtype in this region (Fig-ure 1) Four BVDV-1-positive samples identified in this studywere classified as BVDVndash1m The isolates FS1605 CF1374DF1312 and DB1503 had 945ndash987 homology with eachother and shared 954ndash970homologywith theBVDVndash1mreference strain ZMndash95 (AF526381) (Table 1) Thereforethose four positive samples were clustered into BVDVndash1mBVDVndash1m was first isolated from a diseased pig in 1995 inChina [23] According to a survey conducted between 2005and 2013 this subtype has been widely distributed in Chinaand is the most prevalent among BVDVndash1 subtypes [12]
Our positive samples DS1324 FS1573 and FS1426respectively shared 879 975 and 984 sequence iden-tity with the reference strains BVDVndash1a NADL (M31182)BVDVndash1c Manasi (EU159702) Bega (AF049221) BVDVndash1pTJ06 (GU120246) and TJ07 (GU120247) (Table 1) Thesepositive samples were classified into BVDVndash1a 1c and 1pwhich are not commonly found
In summary this study demonstrated that BVDVndash1was a common causative agent for infection of goats insouthwestern China and that 1751 of the detected samplesfrom ill goats were BVDVndash1 positive However we did notassess samples from the healthy goats and cannot determinethe prevalence of BVDV in healthy goats To further ourunderstanding of the genetic diversity of BVDV strainsdetected all antigen-positive samples were confirmed andcharacterizedwith RT-PCR as being infected by BVDVndash1 butnot BVDVndash2 BVDVndash3 or BDV Twelve BVDVndash1-positivesamples were identified from these RT-PCR positive samplesand were clustered into the six subtypes BVDVndash1a 1b 1c 1mand 1p Due to the possibility of cross infections of BVDVthat might occur among cattle piglets and goats muchmore emphasis should be placed on epidemiology surveysin these animals This is the first description of the geneticdiversity of BVDVndash1-positive samples collected from goats insouthwestern China
Data Availability
The data used to support the findings of this study areincluded within the article
Ethical Approval
No studies involving human participants or animals per-formed by any of authors are described in this article
Conflicts of Interest
The authors declare that there are no conflicts of interest inthis study
Authorsrsquo Contributions
Yu Deng and Guiying Hao designed and performed theexperiments Silu Wang contributed to the clinical diagnosisand collected samples YuDeng and Runxia Liu analyzed dataand wrote the manuscript All authors read and approved thefinal manuscript
Acknowledgments
This study was supported by the Applied FoundationProject of the Sichuan Provincial Science and TechnologyDepartment (2018JY0243) the Key Foundation Project ofthe Sichuan Provincial Education Department (18ZD0442)the ldquoDouble high talentrdquo Project of Xichang College(LGZ201712) and the postdoctoral scholarship of ChinaScholarship council (CSC201408515154)
References
[1] L Liu H Xia NWahlberg S Belak and C Baule ldquoPhylogenyclassification and evolutionary insights into pestivirusesrdquoVirol-ogy vol 385 no 2 pp 351ndash357 2009
[2] F V Bauermann J F Ridpath R Weiblen and E F FloresldquoHoBi-like viruses An emerging group of pestivirusesrdquo Journalof Veterinary Diagnostic Investigation vol 25 no 1 pp 6ndash152013
[3] J F Ridpath ldquoEmerging pestiviruses infecting domestic andwildlife hostsrdquo Animal Health Research Reviews vol 16 no 1pp 55ndash59 2015
[4] D B Smith G Meyers J Bukh et al ldquoProposed revision to thetaxonomy of the genus Pestivirus family Flaviviridaerdquo Journalof General Virology vol 98 no 8 pp 2106ndash2112 2017
[5] J F Ridpath ldquoBovine viral diarrhea virus global statusrdquoVeterinary Clinics of North America Food Animal Practice vol26 no 1 pp 105ndash121 2010
[6] T Passler K P Riddell M A Edmondson et al ldquoExperimentalinfection of pregnant goats with bovine viral diarrhea virus(BVDV) 1 or 2rdquo Veterinary Research vol 45 no 1 p 38 2014
[7] Y Abe T Tamura S Torii et al ldquoGenetic and antigeniccharacterization of bovine viral diarrhea viruses isolated fromcattle inHokkaido Japanrdquo Journal of VeterinaryMedical Sciencevol 78 no 1 pp 61ndash70 2016
[8] MDeng S JiW Fei et al ldquoPrevalence study and genetic typingof Bovine Viral Diarrhea Virus (BVDV) in four bovine speciesin Chinardquo PLoS ONE vol 10 no 4 2015
[9] S Silveira M N Weber A C S Mosena et al ldquoGeneticdiversity of brazilian bovine pestiviruses detected between 1995and 2014rdquo Transboundary and Emerging Diseases vol 64 no 2pp 613ndash623 2017
Journal of Veterinary Medicine 5
[10] L Elvira Partida M Fern Ndez J Guti Rrez et al ldquoDetectionof Bovine Viral Diarrhoea Virus 2 as the Cause of AbortionOutbreaks on Commercial Sheep Flocksrdquo Transboundary andEmerging Diseases vol 64 pp 19ndash26 2017
[11] M JenckelD HoperH Schirrmeier et al ldquoMixed triple Alliedviruses in unique recent isolates of highly virulent type 2 bovineviral diarrhea virus detected by deep sequencingrdquo Journal ofVirology vol 88 no 12 pp 6983ndash6992 2014
[12] K Yesilbag G Alpay and P Becher ldquoVariability and globaldistribution of subgenotypes of bovine viral diarrhea virusrdquoViruses vol 9 p 128 2017
[13] L Mao W Li L Yang et al ldquoPrimary surveys on molecularepidemiology of bovine viral diarrhea virus 1 infecting goats inJiangsu province Chinardquo BMC Veterinary Research vol 12 p181 2016
[14] Y Deng C-Q Sun S-J Cao et al ldquoHigh prevalence ofbovine viral diarrhea virus 1 in Chinese swine herdsrdquoVeterinaryMicrobiology vol 159 no 3-4 pp 490ndash493 2012
[15] M N Weber S Silveira G Machado et al ldquoHigh frequencyof bovine viral diarrhea virus type 2 in Southern Brazilrdquo VirusResearch vol 191 no 1 pp 117ndash124 2014
[16] V Mari M Losurdo M S Lucente et al ldquoMultiplex real-timeRT-PCR assay for bovine viral diarrhea virus type 1 type 2 andHoBi-like pestivirusrdquo Journal of Virological Methods vol 229pp 1ndash7 2016
[17] H Albayrak S O Gumusova E Ozan and Z Yazici ldquoMolecu-lar detection of pestiviruses in aborted foetuses from provincesin northern Turkeyrdquo Tropical Animal Health and Productionvol 44 no 4 pp 677ndash680 2012
[18] S Kumar G Stecher and K Tamura ldquoMEGA7 MolecularEvolutionary Genetics Analysis version 70 for bigger datasetsrdquoMolecular Biology and Evolution vol 33 no 7 pp 1870ndash18742016
[19] D D Nelson M J Dark D S Bradway et al ldquoEvidence forpersistent Bovine viral diarrhea virus infection in a captivemountain goat (Oreamnos americanus)rdquo Journal of VeterinaryDiagnostic Investigation vol 20 no 6 pp 752ndash759 2008
[20] F Xue Y-M Zhu J Li et al ldquoGenotyping of bovine viraldiarrhea viruses from cattle in China between 2005 and 2008rdquoVeterinary Microbiology vol 143 pp 379ndash383 2010
[21] F Zhong N Li X Huang et al ldquoGenetic typing and epidemi-ologic observation of bovine viral diarrhea virus in WesternChinardquo Virus Genes vol 42 no 2 pp 204ndash207 2011
[22] S Gao J Luo J Du et al ldquoSerological and molecular evi-dence for natural infection of Bactrian camels with multiplesubgenotypes of bovine viral diarrhea virus in Western ChinardquoVeterinary Microbiology vol 163 no 1-2 pp 172ndash176 2013
[23] X Xu Q Zhang X Yu et al ldquoSequencing and comparativeanalysis of a pig bovine viral diarrhea virus genomerdquo VirusResearch vol 122 no 1-2 pp 164ndash170 2006
Veterinary MedicineJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
International Journal of
Microbiology
Veterinary Medicine International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
BioMed Research International
EcologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
PsycheHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
Hindawiwwwhindawicom
Applied ampEnvironmentalSoil Science
Volume 2018
Biotechnology Research International
Hindawiwwwhindawicom Volume 2018
Agronomy
Hindawiwwwhindawicom Volume 2018
International Journal of
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y
ScienticaHindawiwwwhindawicom Volume 2018
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Case Reports in Veterinary Medicine
Submit your manuscripts atwwwhindawicom
Journal of Veterinary Medicine 3
Figure 1 Phylogenetic tree of a 224 bp portion of the 51015840-UTR nucleotide sequences The BVDV strains isolated from goats in southwesternChina with Pestivirus reference strains of BVDV-1 BVDV-2 BVDV-3 and BDV registered in GenBank database The tree was constructedusing the Neighbor-Joining method bootstrapping (1000 replications) and the Kimura three parameter statistical model of MEGA 70software The 12 isolated sequences from goat serum in this study are designated with ldquoblue circlerdquo
MN1319) were clustered within BVDVndash1b one (DS1324) wastyped as BVDVndash1a one (FS1573) as BVDVndash1c one (FS1426)as BVDVndash1p and four (FS1605 CF1374 DF1312 andDB1503)were characterized as BVDVndash1m No BVDVndash2 BVDVndash3 orBDV was detected in field isolates by phylogenetic analysis
4 Discussion
In this study we identified 12 selected BVDV-1-positivesamples that represented different flocks or geographicalorigins of blood samples collected between 2013 and 2016
Experimental or natural infection in goats has been previ-ously confirmed [19] Goats infected with BVDV representa great risk for disease transmission thus making the identi-fication of BVDV infection in goats an important endeavorThis investigation described the genetic diversity of BVDVisolated from goats in southwestern China and demonstratedthe occurrence of at least five subtypes of BVDV includingBVDVndash1a 1b 1c 1m and 1p
Among the BVDVndash1 types the most frequent subtypewas BVDVndash1b (n=5) (Table 1 and Figure 1) Five BVDVndash1b-positive samples from different counties of southwestern
4 Journal of Veterinary Medicine
China shared 981ndash990 identity with each other and had916ndash980 identity with the reference strain BVDVndash1b24ndash15 (AF298060) and Osloss (M96687) Those five strainswere also clustered with the two BVDV-1b reference strains(Figure 1) In cattle BVDVndash1b was first detected in thetissue of a bovine fetus in 1980 in China and continu-ally isolated and identified in Tianjin Hebei Gansu Xin-jiang and Heilongjiang province from then onward [8 2021]
The 1b subtype is widely considered to be a majorcontributor to infection in Chinese cattle [20 22] SimilarlyBVDV-1b is also a main subtype in Chinese goat herds[13] BVDV transmission among different animal species hasbeen proven and therefore increased surveillance of BVDVinfection in goats should be an important factor to considerin the control and understanding of BVDV infection incattle
BVDVndash1m is another major subtype in this region (Fig-ure 1) Four BVDV-1-positive samples identified in this studywere classified as BVDVndash1m The isolates FS1605 CF1374DF1312 and DB1503 had 945ndash987 homology with eachother and shared 954ndash970homologywith theBVDVndash1mreference strain ZMndash95 (AF526381) (Table 1) Thereforethose four positive samples were clustered into BVDVndash1mBVDVndash1m was first isolated from a diseased pig in 1995 inChina [23] According to a survey conducted between 2005and 2013 this subtype has been widely distributed in Chinaand is the most prevalent among BVDVndash1 subtypes [12]
Our positive samples DS1324 FS1573 and FS1426respectively shared 879 975 and 984 sequence iden-tity with the reference strains BVDVndash1a NADL (M31182)BVDVndash1c Manasi (EU159702) Bega (AF049221) BVDVndash1pTJ06 (GU120246) and TJ07 (GU120247) (Table 1) Thesepositive samples were classified into BVDVndash1a 1c and 1pwhich are not commonly found
In summary this study demonstrated that BVDVndash1was a common causative agent for infection of goats insouthwestern China and that 1751 of the detected samplesfrom ill goats were BVDVndash1 positive However we did notassess samples from the healthy goats and cannot determinethe prevalence of BVDV in healthy goats To further ourunderstanding of the genetic diversity of BVDV strainsdetected all antigen-positive samples were confirmed andcharacterizedwith RT-PCR as being infected by BVDVndash1 butnot BVDVndash2 BVDVndash3 or BDV Twelve BVDVndash1-positivesamples were identified from these RT-PCR positive samplesand were clustered into the six subtypes BVDVndash1a 1b 1c 1mand 1p Due to the possibility of cross infections of BVDVthat might occur among cattle piglets and goats muchmore emphasis should be placed on epidemiology surveysin these animals This is the first description of the geneticdiversity of BVDVndash1-positive samples collected from goats insouthwestern China
Data Availability
The data used to support the findings of this study areincluded within the article
Ethical Approval
No studies involving human participants or animals per-formed by any of authors are described in this article
Conflicts of Interest
The authors declare that there are no conflicts of interest inthis study
Authorsrsquo Contributions
Yu Deng and Guiying Hao designed and performed theexperiments Silu Wang contributed to the clinical diagnosisand collected samples YuDeng and Runxia Liu analyzed dataand wrote the manuscript All authors read and approved thefinal manuscript
Acknowledgments
This study was supported by the Applied FoundationProject of the Sichuan Provincial Science and TechnologyDepartment (2018JY0243) the Key Foundation Project ofthe Sichuan Provincial Education Department (18ZD0442)the ldquoDouble high talentrdquo Project of Xichang College(LGZ201712) and the postdoctoral scholarship of ChinaScholarship council (CSC201408515154)
References
[1] L Liu H Xia NWahlberg S Belak and C Baule ldquoPhylogenyclassification and evolutionary insights into pestivirusesrdquoVirol-ogy vol 385 no 2 pp 351ndash357 2009
[2] F V Bauermann J F Ridpath R Weiblen and E F FloresldquoHoBi-like viruses An emerging group of pestivirusesrdquo Journalof Veterinary Diagnostic Investigation vol 25 no 1 pp 6ndash152013
[3] J F Ridpath ldquoEmerging pestiviruses infecting domestic andwildlife hostsrdquo Animal Health Research Reviews vol 16 no 1pp 55ndash59 2015
[4] D B Smith G Meyers J Bukh et al ldquoProposed revision to thetaxonomy of the genus Pestivirus family Flaviviridaerdquo Journalof General Virology vol 98 no 8 pp 2106ndash2112 2017
[5] J F Ridpath ldquoBovine viral diarrhea virus global statusrdquoVeterinary Clinics of North America Food Animal Practice vol26 no 1 pp 105ndash121 2010
[6] T Passler K P Riddell M A Edmondson et al ldquoExperimentalinfection of pregnant goats with bovine viral diarrhea virus(BVDV) 1 or 2rdquo Veterinary Research vol 45 no 1 p 38 2014
[7] Y Abe T Tamura S Torii et al ldquoGenetic and antigeniccharacterization of bovine viral diarrhea viruses isolated fromcattle inHokkaido Japanrdquo Journal of VeterinaryMedical Sciencevol 78 no 1 pp 61ndash70 2016
[8] MDeng S JiW Fei et al ldquoPrevalence study and genetic typingof Bovine Viral Diarrhea Virus (BVDV) in four bovine speciesin Chinardquo PLoS ONE vol 10 no 4 2015
[9] S Silveira M N Weber A C S Mosena et al ldquoGeneticdiversity of brazilian bovine pestiviruses detected between 1995and 2014rdquo Transboundary and Emerging Diseases vol 64 no 2pp 613ndash623 2017
Journal of Veterinary Medicine 5
[10] L Elvira Partida M Fern Ndez J Guti Rrez et al ldquoDetectionof Bovine Viral Diarrhoea Virus 2 as the Cause of AbortionOutbreaks on Commercial Sheep Flocksrdquo Transboundary andEmerging Diseases vol 64 pp 19ndash26 2017
[11] M JenckelD HoperH Schirrmeier et al ldquoMixed triple Alliedviruses in unique recent isolates of highly virulent type 2 bovineviral diarrhea virus detected by deep sequencingrdquo Journal ofVirology vol 88 no 12 pp 6983ndash6992 2014
[12] K Yesilbag G Alpay and P Becher ldquoVariability and globaldistribution of subgenotypes of bovine viral diarrhea virusrdquoViruses vol 9 p 128 2017
[13] L Mao W Li L Yang et al ldquoPrimary surveys on molecularepidemiology of bovine viral diarrhea virus 1 infecting goats inJiangsu province Chinardquo BMC Veterinary Research vol 12 p181 2016
[14] Y Deng C-Q Sun S-J Cao et al ldquoHigh prevalence ofbovine viral diarrhea virus 1 in Chinese swine herdsrdquoVeterinaryMicrobiology vol 159 no 3-4 pp 490ndash493 2012
[15] M N Weber S Silveira G Machado et al ldquoHigh frequencyof bovine viral diarrhea virus type 2 in Southern Brazilrdquo VirusResearch vol 191 no 1 pp 117ndash124 2014
[16] V Mari M Losurdo M S Lucente et al ldquoMultiplex real-timeRT-PCR assay for bovine viral diarrhea virus type 1 type 2 andHoBi-like pestivirusrdquo Journal of Virological Methods vol 229pp 1ndash7 2016
[17] H Albayrak S O Gumusova E Ozan and Z Yazici ldquoMolecu-lar detection of pestiviruses in aborted foetuses from provincesin northern Turkeyrdquo Tropical Animal Health and Productionvol 44 no 4 pp 677ndash680 2012
[18] S Kumar G Stecher and K Tamura ldquoMEGA7 MolecularEvolutionary Genetics Analysis version 70 for bigger datasetsrdquoMolecular Biology and Evolution vol 33 no 7 pp 1870ndash18742016
[19] D D Nelson M J Dark D S Bradway et al ldquoEvidence forpersistent Bovine viral diarrhea virus infection in a captivemountain goat (Oreamnos americanus)rdquo Journal of VeterinaryDiagnostic Investigation vol 20 no 6 pp 752ndash759 2008
[20] F Xue Y-M Zhu J Li et al ldquoGenotyping of bovine viraldiarrhea viruses from cattle in China between 2005 and 2008rdquoVeterinary Microbiology vol 143 pp 379ndash383 2010
[21] F Zhong N Li X Huang et al ldquoGenetic typing and epidemi-ologic observation of bovine viral diarrhea virus in WesternChinardquo Virus Genes vol 42 no 2 pp 204ndash207 2011
[22] S Gao J Luo J Du et al ldquoSerological and molecular evi-dence for natural infection of Bactrian camels with multiplesubgenotypes of bovine viral diarrhea virus in Western ChinardquoVeterinary Microbiology vol 163 no 1-2 pp 172ndash176 2013
[23] X Xu Q Zhang X Yu et al ldquoSequencing and comparativeanalysis of a pig bovine viral diarrhea virus genomerdquo VirusResearch vol 122 no 1-2 pp 164ndash170 2006
Veterinary MedicineJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
International Journal of
Microbiology
Veterinary Medicine International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
BioMed Research International
EcologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
PsycheHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
Hindawiwwwhindawicom
Applied ampEnvironmentalSoil Science
Volume 2018
Biotechnology Research International
Hindawiwwwhindawicom Volume 2018
Agronomy
Hindawiwwwhindawicom Volume 2018
International Journal of
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y
ScienticaHindawiwwwhindawicom Volume 2018
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Case Reports in Veterinary Medicine
Submit your manuscripts atwwwhindawicom
4 Journal of Veterinary Medicine
China shared 981ndash990 identity with each other and had916ndash980 identity with the reference strain BVDVndash1b24ndash15 (AF298060) and Osloss (M96687) Those five strainswere also clustered with the two BVDV-1b reference strains(Figure 1) In cattle BVDVndash1b was first detected in thetissue of a bovine fetus in 1980 in China and continu-ally isolated and identified in Tianjin Hebei Gansu Xin-jiang and Heilongjiang province from then onward [8 2021]
The 1b subtype is widely considered to be a majorcontributor to infection in Chinese cattle [20 22] SimilarlyBVDV-1b is also a main subtype in Chinese goat herds[13] BVDV transmission among different animal species hasbeen proven and therefore increased surveillance of BVDVinfection in goats should be an important factor to considerin the control and understanding of BVDV infection incattle
BVDVndash1m is another major subtype in this region (Fig-ure 1) Four BVDV-1-positive samples identified in this studywere classified as BVDVndash1m The isolates FS1605 CF1374DF1312 and DB1503 had 945ndash987 homology with eachother and shared 954ndash970homologywith theBVDVndash1mreference strain ZMndash95 (AF526381) (Table 1) Thereforethose four positive samples were clustered into BVDVndash1mBVDVndash1m was first isolated from a diseased pig in 1995 inChina [23] According to a survey conducted between 2005and 2013 this subtype has been widely distributed in Chinaand is the most prevalent among BVDVndash1 subtypes [12]
Our positive samples DS1324 FS1573 and FS1426respectively shared 879 975 and 984 sequence iden-tity with the reference strains BVDVndash1a NADL (M31182)BVDVndash1c Manasi (EU159702) Bega (AF049221) BVDVndash1pTJ06 (GU120246) and TJ07 (GU120247) (Table 1) Thesepositive samples were classified into BVDVndash1a 1c and 1pwhich are not commonly found
In summary this study demonstrated that BVDVndash1was a common causative agent for infection of goats insouthwestern China and that 1751 of the detected samplesfrom ill goats were BVDVndash1 positive However we did notassess samples from the healthy goats and cannot determinethe prevalence of BVDV in healthy goats To further ourunderstanding of the genetic diversity of BVDV strainsdetected all antigen-positive samples were confirmed andcharacterizedwith RT-PCR as being infected by BVDVndash1 butnot BVDVndash2 BVDVndash3 or BDV Twelve BVDVndash1-positivesamples were identified from these RT-PCR positive samplesand were clustered into the six subtypes BVDVndash1a 1b 1c 1mand 1p Due to the possibility of cross infections of BVDVthat might occur among cattle piglets and goats muchmore emphasis should be placed on epidemiology surveysin these animals This is the first description of the geneticdiversity of BVDVndash1-positive samples collected from goats insouthwestern China
Data Availability
The data used to support the findings of this study areincluded within the article
Ethical Approval
No studies involving human participants or animals per-formed by any of authors are described in this article
Conflicts of Interest
The authors declare that there are no conflicts of interest inthis study
Authorsrsquo Contributions
Yu Deng and Guiying Hao designed and performed theexperiments Silu Wang contributed to the clinical diagnosisand collected samples YuDeng and Runxia Liu analyzed dataand wrote the manuscript All authors read and approved thefinal manuscript
Acknowledgments
This study was supported by the Applied FoundationProject of the Sichuan Provincial Science and TechnologyDepartment (2018JY0243) the Key Foundation Project ofthe Sichuan Provincial Education Department (18ZD0442)the ldquoDouble high talentrdquo Project of Xichang College(LGZ201712) and the postdoctoral scholarship of ChinaScholarship council (CSC201408515154)
References
[1] L Liu H Xia NWahlberg S Belak and C Baule ldquoPhylogenyclassification and evolutionary insights into pestivirusesrdquoVirol-ogy vol 385 no 2 pp 351ndash357 2009
[2] F V Bauermann J F Ridpath R Weiblen and E F FloresldquoHoBi-like viruses An emerging group of pestivirusesrdquo Journalof Veterinary Diagnostic Investigation vol 25 no 1 pp 6ndash152013
[3] J F Ridpath ldquoEmerging pestiviruses infecting domestic andwildlife hostsrdquo Animal Health Research Reviews vol 16 no 1pp 55ndash59 2015
[4] D B Smith G Meyers J Bukh et al ldquoProposed revision to thetaxonomy of the genus Pestivirus family Flaviviridaerdquo Journalof General Virology vol 98 no 8 pp 2106ndash2112 2017
[5] J F Ridpath ldquoBovine viral diarrhea virus global statusrdquoVeterinary Clinics of North America Food Animal Practice vol26 no 1 pp 105ndash121 2010
[6] T Passler K P Riddell M A Edmondson et al ldquoExperimentalinfection of pregnant goats with bovine viral diarrhea virus(BVDV) 1 or 2rdquo Veterinary Research vol 45 no 1 p 38 2014
[7] Y Abe T Tamura S Torii et al ldquoGenetic and antigeniccharacterization of bovine viral diarrhea viruses isolated fromcattle inHokkaido Japanrdquo Journal of VeterinaryMedical Sciencevol 78 no 1 pp 61ndash70 2016
[8] MDeng S JiW Fei et al ldquoPrevalence study and genetic typingof Bovine Viral Diarrhea Virus (BVDV) in four bovine speciesin Chinardquo PLoS ONE vol 10 no 4 2015
[9] S Silveira M N Weber A C S Mosena et al ldquoGeneticdiversity of brazilian bovine pestiviruses detected between 1995and 2014rdquo Transboundary and Emerging Diseases vol 64 no 2pp 613ndash623 2017
Journal of Veterinary Medicine 5
[10] L Elvira Partida M Fern Ndez J Guti Rrez et al ldquoDetectionof Bovine Viral Diarrhoea Virus 2 as the Cause of AbortionOutbreaks on Commercial Sheep Flocksrdquo Transboundary andEmerging Diseases vol 64 pp 19ndash26 2017
[11] M JenckelD HoperH Schirrmeier et al ldquoMixed triple Alliedviruses in unique recent isolates of highly virulent type 2 bovineviral diarrhea virus detected by deep sequencingrdquo Journal ofVirology vol 88 no 12 pp 6983ndash6992 2014
[12] K Yesilbag G Alpay and P Becher ldquoVariability and globaldistribution of subgenotypes of bovine viral diarrhea virusrdquoViruses vol 9 p 128 2017
[13] L Mao W Li L Yang et al ldquoPrimary surveys on molecularepidemiology of bovine viral diarrhea virus 1 infecting goats inJiangsu province Chinardquo BMC Veterinary Research vol 12 p181 2016
[14] Y Deng C-Q Sun S-J Cao et al ldquoHigh prevalence ofbovine viral diarrhea virus 1 in Chinese swine herdsrdquoVeterinaryMicrobiology vol 159 no 3-4 pp 490ndash493 2012
[15] M N Weber S Silveira G Machado et al ldquoHigh frequencyof bovine viral diarrhea virus type 2 in Southern Brazilrdquo VirusResearch vol 191 no 1 pp 117ndash124 2014
[16] V Mari M Losurdo M S Lucente et al ldquoMultiplex real-timeRT-PCR assay for bovine viral diarrhea virus type 1 type 2 andHoBi-like pestivirusrdquo Journal of Virological Methods vol 229pp 1ndash7 2016
[17] H Albayrak S O Gumusova E Ozan and Z Yazici ldquoMolecu-lar detection of pestiviruses in aborted foetuses from provincesin northern Turkeyrdquo Tropical Animal Health and Productionvol 44 no 4 pp 677ndash680 2012
[18] S Kumar G Stecher and K Tamura ldquoMEGA7 MolecularEvolutionary Genetics Analysis version 70 for bigger datasetsrdquoMolecular Biology and Evolution vol 33 no 7 pp 1870ndash18742016
[19] D D Nelson M J Dark D S Bradway et al ldquoEvidence forpersistent Bovine viral diarrhea virus infection in a captivemountain goat (Oreamnos americanus)rdquo Journal of VeterinaryDiagnostic Investigation vol 20 no 6 pp 752ndash759 2008
[20] F Xue Y-M Zhu J Li et al ldquoGenotyping of bovine viraldiarrhea viruses from cattle in China between 2005 and 2008rdquoVeterinary Microbiology vol 143 pp 379ndash383 2010
[21] F Zhong N Li X Huang et al ldquoGenetic typing and epidemi-ologic observation of bovine viral diarrhea virus in WesternChinardquo Virus Genes vol 42 no 2 pp 204ndash207 2011
[22] S Gao J Luo J Du et al ldquoSerological and molecular evi-dence for natural infection of Bactrian camels with multiplesubgenotypes of bovine viral diarrhea virus in Western ChinardquoVeterinary Microbiology vol 163 no 1-2 pp 172ndash176 2013
[23] X Xu Q Zhang X Yu et al ldquoSequencing and comparativeanalysis of a pig bovine viral diarrhea virus genomerdquo VirusResearch vol 122 no 1-2 pp 164ndash170 2006
Veterinary MedicineJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
International Journal of
Microbiology
Veterinary Medicine International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
BioMed Research International
EcologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
PsycheHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
Hindawiwwwhindawicom
Applied ampEnvironmentalSoil Science
Volume 2018
Biotechnology Research International
Hindawiwwwhindawicom Volume 2018
Agronomy
Hindawiwwwhindawicom Volume 2018
International Journal of
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y
ScienticaHindawiwwwhindawicom Volume 2018
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Case Reports in Veterinary Medicine
Submit your manuscripts atwwwhindawicom
Journal of Veterinary Medicine 5
[10] L Elvira Partida M Fern Ndez J Guti Rrez et al ldquoDetectionof Bovine Viral Diarrhoea Virus 2 as the Cause of AbortionOutbreaks on Commercial Sheep Flocksrdquo Transboundary andEmerging Diseases vol 64 pp 19ndash26 2017
[11] M JenckelD HoperH Schirrmeier et al ldquoMixed triple Alliedviruses in unique recent isolates of highly virulent type 2 bovineviral diarrhea virus detected by deep sequencingrdquo Journal ofVirology vol 88 no 12 pp 6983ndash6992 2014
[12] K Yesilbag G Alpay and P Becher ldquoVariability and globaldistribution of subgenotypes of bovine viral diarrhea virusrdquoViruses vol 9 p 128 2017
[13] L Mao W Li L Yang et al ldquoPrimary surveys on molecularepidemiology of bovine viral diarrhea virus 1 infecting goats inJiangsu province Chinardquo BMC Veterinary Research vol 12 p181 2016
[14] Y Deng C-Q Sun S-J Cao et al ldquoHigh prevalence ofbovine viral diarrhea virus 1 in Chinese swine herdsrdquoVeterinaryMicrobiology vol 159 no 3-4 pp 490ndash493 2012
[15] M N Weber S Silveira G Machado et al ldquoHigh frequencyof bovine viral diarrhea virus type 2 in Southern Brazilrdquo VirusResearch vol 191 no 1 pp 117ndash124 2014
[16] V Mari M Losurdo M S Lucente et al ldquoMultiplex real-timeRT-PCR assay for bovine viral diarrhea virus type 1 type 2 andHoBi-like pestivirusrdquo Journal of Virological Methods vol 229pp 1ndash7 2016
[17] H Albayrak S O Gumusova E Ozan and Z Yazici ldquoMolecu-lar detection of pestiviruses in aborted foetuses from provincesin northern Turkeyrdquo Tropical Animal Health and Productionvol 44 no 4 pp 677ndash680 2012
[18] S Kumar G Stecher and K Tamura ldquoMEGA7 MolecularEvolutionary Genetics Analysis version 70 for bigger datasetsrdquoMolecular Biology and Evolution vol 33 no 7 pp 1870ndash18742016
[19] D D Nelson M J Dark D S Bradway et al ldquoEvidence forpersistent Bovine viral diarrhea virus infection in a captivemountain goat (Oreamnos americanus)rdquo Journal of VeterinaryDiagnostic Investigation vol 20 no 6 pp 752ndash759 2008
[20] F Xue Y-M Zhu J Li et al ldquoGenotyping of bovine viraldiarrhea viruses from cattle in China between 2005 and 2008rdquoVeterinary Microbiology vol 143 pp 379ndash383 2010
[21] F Zhong N Li X Huang et al ldquoGenetic typing and epidemi-ologic observation of bovine viral diarrhea virus in WesternChinardquo Virus Genes vol 42 no 2 pp 204ndash207 2011
[22] S Gao J Luo J Du et al ldquoSerological and molecular evi-dence for natural infection of Bactrian camels with multiplesubgenotypes of bovine viral diarrhea virus in Western ChinardquoVeterinary Microbiology vol 163 no 1-2 pp 172ndash176 2013
[23] X Xu Q Zhang X Yu et al ldquoSequencing and comparativeanalysis of a pig bovine viral diarrhea virus genomerdquo VirusResearch vol 122 no 1-2 pp 164ndash170 2006
Veterinary MedicineJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
International Journal of
Microbiology
Veterinary Medicine International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
BioMed Research International
EcologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
PsycheHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
Hindawiwwwhindawicom
Applied ampEnvironmentalSoil Science
Volume 2018
Biotechnology Research International
Hindawiwwwhindawicom Volume 2018
Agronomy
Hindawiwwwhindawicom Volume 2018
International Journal of
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y
ScienticaHindawiwwwhindawicom Volume 2018
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Case Reports in Veterinary Medicine
Submit your manuscripts atwwwhindawicom
Veterinary MedicineJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
International Journal of
Microbiology
Veterinary Medicine International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
BioMed Research International
EcologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
PsycheHindawiwwwhindawicom Volume 2018
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