The circulation of arboviruses in livestock ruminants has often gone unrecognized owing to the fact that a significant percentage of arboviruses probably induce subclinical infections and/or negligible symptoms in infected animals. To determine the current situation of arbovirus circulation in the Yaeyama Islands, attempts to isolate viruses from bovine blood samples collected between 2014 and 2019 have been made. In total, 308 blood samples were collected during the study period, and 43 of them induced cytopathic effects (CPEs) in cell cultures. The identification of the CPE agents was performed by reported RT-PCR assays and a high-throughput analysis with a next-generation sequencing platform. The obtained viruses consisted of an orthobunyavirus (Peaton virus), Culicoides-borne orbiviruses (bluetongue virus serotypes 12 and 16, epizootic hemorrhagic disease virus [EHDV] serotypes 5, 6, and 7, D'Aguilar virus, and Bunyip Creek virus), and potential mosquito-borne orbiviruses (Yunnan orbivirus, Guangxi orbivirus, and Yonaguni orbivirus). Most of the orbiviruses were recovered from washed blood cells with mosquito cell cultures, suggesting that this combination was more efficient than other combinations such as plasma/blood cells and hamster cell lines. This marked the first time that the isolation of EHDV serotypes 5 and 6 and three potential mosquito-borne orbiviruses was recorded in Japan, showing a greater variety of orbiviruses on the islands than previously known. Genetic analysis of the isolated orbiviruses suggested that the Yaeyama Islands and its neighboring regions were epidemiologically related. Some of the viruses, especially the potential mosquito-borne orbiviruses, were isolated during several consecutive years, indicating their establishment on the islands.
Get full access to this article
View all access options for this article.
References
1.
AhasanMS, SubramaniamK, Campos KrauerJM, SaylerKA, et al.Three new orbivirus species isolated from farmed white-tailed deer (Odocoileus virginianus) in the United States. Viruses, 2019; 12:13.
2.
AizawaM, TakayoshiK, KokubaT, KatoT, et al.Molecular epidemiological analysis of bovine ephemeral fever virus isolated in Okinawa Prefecture. J Jpn Vet Med Assoc, 2008; 61:363–366.
AttouiH, JaafarFM, BelhouchetM, AldrovandiN, et al.Yunnan orbivirus, a new orbivirus species isolated from Culex tritaeniorhynchus mosquitoes in China. J Gen Virol, 2005; 86:3409–3417.
5.
AttouiH, Mendez-LopezMR, RaoS, Hurtado-AlendesA, et al.Peruvian horse sickness virus and Yunnan orbivirus, isolated from vertebrates and mosquitoes in Peru and Australia. Virology, 2009; 394:298–310.
6.
CooperE, AnbalaganS, KlumperP, ScherbaG, et al.Mobuck virus genome sequence and phylogenetic analysis: Identification of a novel orbivirus isolated from a white-tailed deer in Missouri, USA. J Gen Virol, 2014; 95:110–116.
7.
CowledC, MelvilleL, WeirR, WalshS, et al.Genetic and epidemiological characterization of Middle Point orbivirus, a novel virus isolated from sentinel cattle in northern Australia. J Gen Virol, 2007; 88:3413–3422.
8.
DanielsP, LuntR, PrichardI. Bluetongue in Australia and East Asia. In: MellorPS, BaylisM, MertensPPC, eds. Bluetongue. Paris: Elsevier, 2009:223–234.
9.
EbersohnK, CoetzeeP, SnymanLP, SwanepoelR, et al.Phylogenetic characterization of the Palyam serogroup orbiviruses. Viruses, 2019; 11:446.
10.
ElbersAR, KoenraadtCJ, MeiswinkelR. Mosquitoes and Culicoides biting midges: Vector range and the influence of climate change. Rev Sci Tech, 2015; 34:123–137.
11.
ElliottRM, WilkieML. Persistent infection of Aedes albopictus C6/36 cells by Bunyamwera virus. Virology, 1986; 150:21–32.
12.
EschbaumerM, WernikeK, BattenCA, SaviniG, et al.Epizootic hemorrhagic disease virus serotype 7 in European cattle and sheep: Diagnostic considerations and effect of previous BTV exposure. Vet Microbiol, 2012; 159:298–306.
13.
GardGP, ShorthoseJE, WeirRP, WalshSJ, et al.Arboviruses recovered from sentinel livestock in northern Australia. Vet Microbiol, 1988a; 18:109–118.
14.
GardGP, WeirRP, WalshSJ. Arboviruses recovered from sentinel cattle using several virus isolation methods. Vet Microbiol, 1988b; 18:119–125.
15.
GotoY, MiuraY, KonoY. Serologic evidence for the etiologic role of Chuzan virus in an epizootic of congenital abnormalities with hydranencephaly-cerebellar hypoplasia syndrome of calves in Japan. Am J Vet Res, 1988; 49:2026–2029.
16.
GopurenkoD, BellisGA, YanaseT, WardhanaAH, et al.Integrative taxonomy to investigate species boundaries within Culicoides (Diptera: Ceratopogonidae): A case study using subgenus Avaritia from Australasia and Eastern Asia. Vet Ital, 2015; 51:345–378.
17.
GublerDJ, VasilakisN. The arboviruses: Quo Vadis? In: Vasilakis N, Gubler DJ, eds. Arboviruses. Norfolk: Caister Academic Press, 2016:1–6.
18.
HanHD. Propagation and persistent infection of Akabane virus in cultured mosquito cells. Nihon Juigaku Zasshi, 1981; 43:689–697.
19.
HayamaY, MoriguchiS, YanaseT, SuzukiM, et al.Epidemiological analysis of bovine ephemeral fever in 2012–2013 in the subtropical islands of Japan. BMC Vet Res, 2016; 12:47.
20.
HigaY, TomaT, ArakiY, OnoderaI, et al.Seasonal changes in oviposition activity, hatching and embryonation rates of eggs of Aedes albopictus (Diptera: Culicidae) on three islands of the Ryukyu Archipelago, Japan. Med Entomol Zool, 2007; 58:1–10.
21.
HirashimaY, KatoT, YamakawaM, ShirafujiH, et al.Reemergence of Ibaraki disease in southern Japan in 2013. J Vet Med Sci, 2015; 77:1253–1259.
22.
HoshinoC. Notes on biting midges collected by light traps at a cowshed in Ishigaki-jima, Ryukyu Islands. Med Entomol Zool, 1985; 36:55–58.
23.
HwangJM, KimJG, YehJY. Serological evidence of bluetongue virus infection and serotype distribution in dairy cattle in South Korea. BMC Vet Res, 2019; 5:255.
KatoT, AizawaM, TakayoshiK, KokubaT, et al.Phylogenetic relationships of the G gene sequence of bovine ephemeral fever virus isolated in Japan, Taiwan and Australia. Vet Microbiol, 2009; 137:217–223.
26.
KatoT, AizawaM, TakayoshiK, YanaseT, et al.Full genome sequence of a Sathuvachari virus strain isolated in the southwestern-most archipelago of Japan. Virus Genes, 2018; 54:729–732.
27.
KatoT, ShirafujiH, TanakaS, SatoM, et al.Bovine arboviruses in Culicoides biting midges and sentinel cattle in southern Japan from 2003 to 2013. Transbound Emerg Dis, 2016a; 63:e160–e172.
28.
KatoT, YanaseT, SuzukiM, KatagiriY, et al.Monitoring for bovine arboviruses in the most southwestern islands in Japan between 1994 and 2014. BMC Vet Res, 2016b; 12:125.
KumarS, StecherG, LiM, KnyazC, et al.MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 2018; 35:1547–1549.
31.
LeeF, TingLJ, JongMH, ChangWM, et al.Subclinical bluetongue virus infection in domestic ruminants in Taiwan. Vet Microbiol, 2010; 142:225–231.
32.
LiZ, YuM, ZhangH, WangHY, et al.Improved rapid amplification of cDNA ends (RACE) for mapping both the 5′ and 3′ terminal sequences of paramyxovirus genomes. J Virol Methods, 2005; 130:154–156.
33.
MaanNS, MaanS, BelaganahalliMN, OstlundEN, et al.Identification and differentiation of the twenty six bluetongue virus serotypes by RT-PCR amplification of the serotype-specific genome segment 2. PLoS One, 2012; 7:e32601.
34.
MaanNS, MaanS, NomikouK, JohnsonDJ, et al.RT-PCR assays for seven serotypes of epizootic haemorrhagic disease virus & their use to type strains from the Mediterranean region and North America. PLoS One, 2010; 5:e12782.
35.
MaanS, MaanNS, BelaganahalliMN, PotgieterAC, et al.Development and evaluation of real time RT-PCR assays for detection and typing of bluetongue virus. PLoS One. 2016; 11:e0163014.
36.
MaclachlanNJ, ZientaraS, WilsonWC, RichtJA, et al.Bluetongue and epizootic hemorrhagic disease viruses: Recent developments with these globally re-emerging arboviral infections of ruminants. Curr Opin Virol, 2019; 34:56–62.
37.
Méndez-LópezMR, AttouiH, FlorinD, CalisherCH, et al.Association of vectors and environmental conditions during the emergence of Peruvian horse sickness orbivirus and Yunnan orbivirus in northern Peru. J Vec Eco, 2015; 40:355–363.
38.
MurotaK, SudaY, ShirafujiH, IshiiK, et al.Identification and characterization of a novel orbivirus, Yonaguni orbivirus, isolated from cattle on the westernmost island of Japan. Arch Virol, 2020; 165:2903–2908.
39.
NiwaT, ShirafujiH, IkemiyagiK, NittaY, et al.Occurrence of bovine ephemeral fever in Okinawa Prefecture, Japan, in 2012 and development of a reverse-transcription polymerase chain reaction assay to detect bovine ephemeral fever virus gene. J Vet Med Sci, 2015; 77:455–460.
40.
OhashiS, MatsumoriY, YanaseT, YamakawaM, et al.Evidence of an antigenic shift among Palyam serogroup orbiviruses. J Clin Microbiol, 2004a; 42:4610–4614.
41.
OhashiS, YoshidaK, YanaseT, KatoT, et al.Simultaneous detection of bovine arboviruses using single-tube multiplex reverse transcription-polymerase chain reaction. J Virol Methods, 2004b; 120:79–85.
42.
OhashiS, YoshidaK, WatanabeY, TsudaT. Identification and PCR-restriction fragment length polymorphism analysis of a variant of the Ibaraki virus from naturally infected cattle and aborted fetuses in Japan. J Clin Microbiol, 1999; 37:3800–3803.
43.
PrasadG, SreenivasuluD, SinghKP, MertensPPC, et al.Bluetongue in the Indian subcontinent. In: MellorPS, BaylisM, MertensPPC, eds. Bluetongue. Paris: Elsevier, 2009:167–195.
44.
Purnomo EdiS, IbrahimA, SukocoR, BunaliL, et al.Molecular characterization of an Akabane virus isolate from West Java, Indonesia. J Vet Med Sci, 2017; 79:774–779.
45.
QiY, WangF, ChangJ, ZhangY, et al.Identification and complete-genome phylogenetic analysis of an epizootic hemorrhagic disease virus serotype 7 strain isolated in China. Arch Virol, 2019; 164:3121–3126.
46.
RaclozV, GriotC, StärkKD. Sentinel surveillance systems with special focus on vector-borne diseases. Anim Health Res Rev, 2006; 7:71–79.
47.
RiesC, SharavT, Tseren-OchirEO, BeerM, et al.Putative novel serotypes ‘33’ and ‘35’ in clinically healthy small ruminants in Mongolia expand the group of atypical BTV. Viruses, 2020; 29:42.
48.
SadeghiM, PopovV, GuzmanH, PhanTG, et al.Genomes of viral isolates derived from different mosquitos species. Virus Res, 2017; 242:49–57.
49.
SaviniG, AfonsoA, MellorP, AradaibI, et al.Epizootic heamorragic disease. Res Vet Sci, 2011; 91:1–17.
50.
SendowI, DanielsPW, CybinskiDH, YoungPL, et al.Antibodies against certain bluetongue and epizootic haemorrhagic disease viral serotypes in Indonesian ruminants. Vet Microbiol, 1991; 28:111–118.
51.
ShirafujiH, KatoT, YamakawaM, TanakaT, et al.Characterization of genome segments 2, 3 and 6 of epizootic hemorrhagic disease virus strains isolated in Japan in 1985–2013: Identification of their serotypes and geographical genetic types. Infect Genet Evol, 2017; 53:38–46.
52.
ShirafujiH, YanaseT, KatoT, YamakawaM. Genetic and phylogenetic characterization of genome segments 2 and 6 of bluetongue virus isolates in Japan from 1985 to 2008. J Gen Virol, 2012; 93:1465–1473.
53.
SingerRS, MacLachlanNJ, CarpenterTE, 2001. Maximal predicted duration of viremia in bluetongue virus-infected cattle. J Vet Diagn Invest, 2001; 13:43–49.
54.
SunEC, HuangLP, XuQY, WangHX, et al.Emergence of a novel bluetongue virus serotype, China 2014. Transbound Emerg Dis, 2016; 63:585–589.
55.
TairaK, TomaT, TamashiroM, MiyagiI. DNA barcoding for identification of mosquitoes (Diptera: Culicidae) from the Ryukyu Archipelago, Japan. Med Entomol Zool, 2012; 63:289–306.
56.
TamashiroM, TomaT, MannenK, HigaY, et al.Bloodmeal identification and feeding habits of mosquitoes (Diptera: Culicidae) collected at five islands in the Ryukyu Archipelago, Japan. Med Entomol Zool, 2011; 62:53–70.
57.
TomaT, MiyagiI, MalenganishoWLM, MurakamiH, et al.Distribution and seasonal occurrence of Anopheles minimus in Ishigaki Island, Ryukyu Archipelago, Japan, 1998–1999. Med Entomol Zool, 2002; 53(Suppl. 2):29–42.
58.
WadaY, MiyagiI, TakagiM, TsudaY. An annotated list of Culicoides biting midges in Yaeyama Islands in the Southern Part of Japan (Diptera: Ceratopogonidae). Trop Med, 1996; 38:61–68.
59.
WangJ, ZhangH, SunX, FuS, et al.Distribution of mosquitoes and mosquito-borne arboviruses in Yunnan Province near the China-Myanmar-Laos border. Am J Trop Med Hyg, 2011; 84:738–746.
60.
WechslerSJ, McHollandLE. Susceptibilities of 14 cell lines to bluetongue virus infection. J Clin Microbiol, 1988; 26:2324–2327.
61.
YanaseT, KatoT, KatagiriY, AizawaM, et al.Isolation and characterization of bluetongue virus from Culicoides brevitarsis (Diptera: Ceratopogonidae). Med Entomol Zool, 2010; 61:85–91.
62.
YanaseT, KatoT, KuboT, YoshidaK, et al.Isolation of bovine arboviruses from Culicoides biting midges (Diptera: Ceratopogonidae) in southern Japan: 1985–2002. J Med Entomol, 2005; 42:63–67.
63.
YanaseT, MurotaK, HayamaY. Endemic and emerging arboviruses in domestic ruminants in East Asia. Front Vet Sci, 2020; 7:168.
64.
YangH, LiZ, WangJ, LiZ, et al.Novel serotype of epizootic hemorrhagic disease virus, China. Emerg Infect Dis, 2020; 26:3081–3083.
65.
YangH, LiZ, ZhangY, GaoL, et al.Isolation and genomic characterization of a novel orbivirus strain from the blood of cattle. Chin J Virol, 2018; 34:75–84.
66.
ZhangN, MacLachlanNJ, BonneauKR, ZhuJ, et al.Identification of seven serotypes of bluetongue virus from the People's Republic of China. Vet Rec, 1999; 145:427–429.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
