Characterization of canine coronavirus spread among domestic dogs in Vietnam
Identifieur interne : 000946 ( Pmc/Corpus ); précédent : 000945; suivant : 000947Characterization of canine coronavirus spread among domestic dogs in Vietnam
Auteurs : Dung Van Nguyen ; Yukata Terada ; Shohei Minami ; Kenzo Yonemitsu ; Nao Nagata ; Thanh Dinh Ha Le ; Ryusei Kuwata ; Hiroshi Shimoda ; Ken MaedaSource :
- The Journal of Veterinary Medical Science [ 0916-7250 ] ; 2016.
Abstract
Canine coronavirus (CCoV) is an important pathogen that causes enteritis in dogs, but
there is no information on CCoV infection in Vietnam. To examine the prevalence of CCoV
infection among Vietnamese dogs, 201 serum samples were analyzed by virus-neutralization
(VN) test. The results showed that antibody against CCoV-II was present in 87 dogs
(43.3%). To detect genes of CCoV, fecal samples collected from 30 diarrheic and 50 healthy
dogs were examinated by RT-PCR, confirming that 2 diarrheic dogs and 5 healthy dogs were
positive for CCoV. Nucleotide sequences of
Url:
DOI: 10.1292/jvms.16-0538
PubMed: 27840394
PubMed Central: 5326940
Links to Exploration step
PMC:5326940Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Characterization of canine coronavirus spread among domestic dogs in
Vietnam</title><author><name sortKey="Van Nguyen, Dung" sort="Van Nguyen, Dung" uniqKey="Van Nguyen D" first="Dung" last="Van Nguyen">Dung Van Nguyen</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Terada, Yukata" sort="Terada, Yukata" uniqKey="Terada Y" first="Yukata" last="Terada">Yukata Terada</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Minami, Shohei" sort="Minami, Shohei" uniqKey="Minami S" first="Shohei" last="Minami">Shohei Minami</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Yonemitsu, Kenzo" sort="Yonemitsu, Kenzo" uniqKey="Yonemitsu K" first="Kenzo" last="Yonemitsu">Kenzo Yonemitsu</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nagata, Nao" sort="Nagata, Nao" uniqKey="Nagata N" first="Nao" last="Nagata">Nao Nagata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Le, Thanh Dinh Ha" sort="Le, Thanh Dinh Ha" uniqKey="Le T" first="Thanh Dinh Ha" last="Le">Thanh Dinh Ha Le</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Kuwata, Ryusei" sort="Kuwata, Ryusei" uniqKey="Kuwata R" first="Ryusei" last="Kuwata">Ryusei Kuwata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Shimoda, Hiroshi" sort="Shimoda, Hiroshi" uniqKey="Shimoda H" first="Hiroshi" last="Shimoda">Hiroshi Shimoda</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Maeda, Ken" sort="Maeda, Ken" uniqKey="Maeda K" first="Ken" last="Maeda">Ken Maeda</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27840394</idno><idno type="pmc">5326940</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5326940</idno><idno type="RBID">PMC:5326940</idno><idno type="doi">10.1292/jvms.16-0538</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000946</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000946</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Characterization of canine coronavirus spread among domestic dogs in
Vietnam</title><author><name sortKey="Van Nguyen, Dung" sort="Van Nguyen, Dung" uniqKey="Van Nguyen D" first="Dung" last="Van Nguyen">Dung Van Nguyen</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Terada, Yukata" sort="Terada, Yukata" uniqKey="Terada Y" first="Yukata" last="Terada">Yukata Terada</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Minami, Shohei" sort="Minami, Shohei" uniqKey="Minami S" first="Shohei" last="Minami">Shohei Minami</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Yonemitsu, Kenzo" sort="Yonemitsu, Kenzo" uniqKey="Yonemitsu K" first="Kenzo" last="Yonemitsu">Kenzo Yonemitsu</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nagata, Nao" sort="Nagata, Nao" uniqKey="Nagata N" first="Nao" last="Nagata">Nao Nagata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Le, Thanh Dinh Ha" sort="Le, Thanh Dinh Ha" uniqKey="Le T" first="Thanh Dinh Ha" last="Le">Thanh Dinh Ha Le</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Kuwata, Ryusei" sort="Kuwata, Ryusei" uniqKey="Kuwata R" first="Ryusei" last="Kuwata">Ryusei Kuwata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Shimoda, Hiroshi" sort="Shimoda, Hiroshi" uniqKey="Shimoda H" first="Hiroshi" last="Shimoda">Hiroshi Shimoda</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Maeda, Ken" sort="Maeda, Ken" uniqKey="Maeda K" first="Ken" last="Maeda">Ken Maeda</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Veterinary Medical Science</title><idno type="ISSN">0916-7250</idno><idno type="eISSN">1347-7439</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Canine coronavirus (CCoV) is an important pathogen that causes enteritis in dogs, but
there is no information on CCoV infection in Vietnam. To examine the prevalence of CCoV
infection among Vietnamese dogs, 201 serum samples were analyzed by virus-neutralization
(VN) test. The results showed that antibody against CCoV-II was present in 87 dogs
(43.3%). To detect genes of CCoV, fecal samples collected from 30 diarrheic and 50 healthy
dogs were examinated by RT-PCR, confirming that 2 diarrheic dogs and 5 healthy dogs were
positive for CCoV. Nucleotide sequences of <italic>N</italic>-terminal region of spike (S)
gene indicated that CCoV strains were divided into two subgenotypes, CCoV-IIa and -IIb,
respectively. Furthemore, we succeeded in isolating CCoV/dog/HCM47/2015, the isolate was
plaque-purified three times, and 3’-terminal one-third of the genome was analyzed.
Interestingly, the plaque-purified virus had a large deletion in ORF3abc and E genes
(1,165 nt), and a short deletion in ORF7b gene (60 nt), suggesting that these regions are
not necessary for <italic>in vitro</italic> replication of CCoV. Next, the antigenicity
between the isolated CCoV-IIb and the other CCoV-IIa was compared by VN test, revealing
that antigenicty of the isolated CCoV is equal or higher than that of the other CCoV. In
summary, two subgenotypes of CCoV-II are spreading among Vietnamese dogs. The isolated
virus with a large deletion after <italic>in vitro</italic> passage may be useful for the
development of vaccine, owing to its antigenicity and efficient viral growth <italic>in
vitro</italic>.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bandai, C" uniqKey="Bandai C">C. Bandai</name></author><author><name sortKey="Ishiguro, S" uniqKey="Ishiguro S">S. Ishiguro</name></author><author><name sortKey="Masuya, N" uniqKey="Masuya N">N. Masuya</name></author><author><name sortKey="Hohdatsu, T" uniqKey="Hohdatsu T">T. Hohdatsu</name></author><author><name sortKey="Mochizuki, M" uniqKey="Mochizuki M">M. Mochizuki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Balint, A" uniqKey="Balint A">Á. Bálint</name></author><author><name sortKey="Farsang, A" uniqKey="Farsang A">A. Farsang</name></author><author><name sortKey="Zadori, Z" uniqKey="Zadori Z">Z. Zádori</name></author><author><name sortKey="Hornyak, A" uniqKey="Hornyak A">Á. Hornyák</name></author><author><name sortKey="Dencso, L" uniqKey="Dencso L">L. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Vet Med Sci</journal-id><journal-id journal-id-type="iso-abbrev">J. Vet. Med. Sci</journal-id><journal-id journal-id-type="publisher-id">JVMS</journal-id><journal-title-group><journal-title>The Journal of Veterinary Medical Science</journal-title></journal-title-group><issn pub-type="ppub">0916-7250</issn><issn pub-type="epub">1347-7439</issn><publisher><publisher-name>The Japanese Society of Veterinary Science</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27840394</article-id><article-id pub-id-type="pmc">5326940</article-id><article-id pub-id-type="publisher-id">16-0538</article-id><article-id pub-id-type="doi">10.1292/jvms.16-0538</article-id><article-categories><subj-group subj-group-type="heading"><subject>Virology</subject><subj-group><subject>Full Paper</subject></subj-group></subj-group></article-categories><title-group><article-title>Characterization of canine coronavirus spread among domestic dogs in
Vietnam</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>van NGUYEN</surname><given-names>Dung</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>TERADA</surname><given-names>Yukata</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>MINAMI</surname><given-names>Shohei</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>YONEMITSU</surname><given-names>Kenzo</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>NAGATA</surname><given-names>Nao</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>LE</surname><given-names>Thanh Dinh Ha</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>KUWATA</surname><given-names>Ryusei</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>SHIMODA</surname><given-names>Hiroshi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>MAEDA</surname><given-names>Ken</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref rid="cor1" ref-type="corresp"><sup>*</sup></xref></contrib><aff id="aff1"><label>1)</label>Laboratory of Veterinary Microbiology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan</aff><aff id="aff2"><label>2)</label>Veterinary Diagnostic Laboratory, Sub-Department of Animal Health of Ho Chi Minh City, 151 Ly Thuong Kiet, District 11, Ho Chi Minh City, Vietnam</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Correspondence to: Maeda, K., Laboratory of Veterinary
Microbiology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida,
Yamaguchi 753-8515, Japan. e-mail: <email xlink:href="kmaeda@yamaguchi-u.ac.jp">kmaeda@yamaguchi-u.ac.jp</email></corresp></author-notes><pub-date pub-type="epub"><day>14</day><month>11</month><year>2016</year></pub-date><pub-date pub-type="ppub"><month>2</month><year>2017</year></pub-date><volume>79</volume><issue>2</issue><fpage>343</fpage><lpage>349</lpage><history><date date-type="received"><day>17</day><month>10</month><year>2016</year></date><date date-type="accepted"><day>01</day><month>11</month><year>2016</year></date></history><permissions><copyright-statement>©2017 The Japanese Society of Veterinary Science</copyright-statement><copyright-year>2017</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative
Commons Attribution Licene (CC-BY-NC-ND 4.0: <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">http://creativecommons.org/licenses/by-nc-nd/4.0/</ext-link>. </license-p></license></permissions><abstract><p>Canine coronavirus (CCoV) is an important pathogen that causes enteritis in dogs, but
there is no information on CCoV infection in Vietnam. To examine the prevalence of CCoV
infection among Vietnamese dogs, 201 serum samples were analyzed by virus-neutralization
(VN) test. The results showed that antibody against CCoV-II was present in 87 dogs
(43.3%). To detect genes of CCoV, fecal samples collected from 30 diarrheic and 50 healthy
dogs were examinated by RT-PCR, confirming that 2 diarrheic dogs and 5 healthy dogs were
positive for CCoV. Nucleotide sequences of <italic>N</italic>-terminal region of spike (S)
gene indicated that CCoV strains were divided into two subgenotypes, CCoV-IIa and -IIb,
respectively. Furthemore, we succeeded in isolating CCoV/dog/HCM47/2015, the isolate was
plaque-purified three times, and 3’-terminal one-third of the genome was analyzed.
Interestingly, the plaque-purified virus had a large deletion in ORF3abc and E genes
(1,165 nt), and a short deletion in ORF7b gene (60 nt), suggesting that these regions are
not necessary for <italic>in vitro</italic> replication of CCoV. Next, the antigenicity
between the isolated CCoV-IIb and the other CCoV-IIa was compared by VN test, revealing
that antigenicty of the isolated CCoV is equal or higher than that of the other CCoV. In
summary, two subgenotypes of CCoV-II are spreading among Vietnamese dogs. The isolated
virus with a large deletion after <italic>in vitro</italic> passage may be useful for the
development of vaccine, owing to its antigenicity and efficient viral growth <italic>in
vitro</italic>.</p></abstract><kwd-group><kwd>coronavirus</kwd><kwd>dog</kwd><kwd>genotype</kwd></kwd-group></article-meta></front><body><p>Canine coronavirus (CCoV) was first recognized in an outbreak of gastroenteritis among dogs
in 1971 [<xref rid="r4" ref-type="bibr">4</xref>]. Since then, CCoV infection has been
reported in dogs in many countries [<xref rid="r5" ref-type="bibr">5</xref>, <xref rid="r7" ref-type="bibr">7</xref>, <xref rid="r9" ref-type="bibr">9</xref>, <xref rid="r12" ref-type="bibr">12</xref>, <xref rid="r17" ref-type="bibr">17</xref>, <xref rid="r25" ref-type="bibr">25</xref>, <xref rid="r28" ref-type="bibr">28</xref>, <xref rid="r29" ref-type="bibr">29</xref>, <xref rid="r32" ref-type="bibr">32</xref>]. To date,
however, information on CCoV in Vietnam has been unavailable.</p><p>CCoV is a single-stranded, positive-sense RNA virus that belongs to the genus
<italic>Alphacoronavirus</italic>. CCoV was divided into two genotypes, CCoV type I (CCoV-I)
and CCoV type II (CCoV-II), which can be differentiated by nucleotide sequences of the spike
(S) gene and the presence of ORF3 located downstream of the S gene [<xref rid="r6" ref-type="bibr">6</xref>, <xref rid="r22" ref-type="bibr">22</xref>]. CCoV-II is also divided into
two subgenotypes, CCoV-IIa and CCoV-IIb, based on the amino acid sequence of the
<italic>N</italic>-terminal region of the S protein. In the <italic>N</italic>-terminal
region of the S protein of CCoV-IIb, the amino acid sequences are highly similar to those of
transmissible gastroenteritis viruses (TGEV) [<xref rid="r14" ref-type="bibr">14</xref>, <xref rid="r16" ref-type="bibr">16</xref>, <xref rid="r23" ref-type="bibr">23</xref>].</p><p>In this study, the prevalence of CCoV infection among domestic dogs in Vietnam was examined,
and Vietnamese CCoVs were genetically and antigenically characterized.</p><sec sec-type="materials|methods" id="s1"><title>MATERIALS AND METHODS</title><sec><title>Fecal swabs</title><p>A total of 80 fecal swabs were collected from 30 diarrheic and 50 healthy dogs in animal
hospitals and households, respectively, in Ho Chi Minh City in Vietnam from 2013 to 2015.
Their ages ranged from 2 months to 13 years. Swab samples were dissolved in 2
m<italic>l</italic> of phosphate-buffer saline (PBS), filtrated through a
0.22-<italic>µ</italic>m filter (Millipore, Carrigtwohill, Ireland) and stored at −80°C
until analysis.</p></sec><sec><title>Sera</title><p>A total of 201 serum samples were collected from healthy dogs in different districts in
Ho Chi Minh City from 2013 to 2015 and stored at −20°C until analysis.</p></sec><sec><title>Viral RNA extraction</title><p>RNA was extracted from CCoV-infected cells and filtrated fecal swabs using RNeasy Mini
kit (Qiagen, Hilden, Germany) and Viral RNA Mini Kit (Qiagen), respectively.</p></sec><sec><title>Reverse transciption-polymerase chain reaction (RT-PCR)</title><p>RT-PCR was performed using QIAGEN One step RT-PCR (Qiagen). The primer sets ORF3F, 5′-CAC
TAA ACT CAA AAT GTT GAT TC-3′ and ORF3R, 5′-TTA AGG ATT AAA AAC ATA TTC TA-3′ [<xref rid="r15" ref-type="bibr">15</xref>] and 2bF, 5′-AGG TTG TTG TGG ATG CAT AG-3′ and 2bR,
5′-ACG GTC AAG TTC GTC AAG TA-3′ [<xref rid="r3" ref-type="bibr">3</xref>], were used for
detection of CCoV-I and CCoV-II, respectively. Amplified products were confirmed as 628 bp
for CCoV-I and 232 bp for CCoV-II by electrophoresis on 2% agarose gels and were then
purified using QIAquick PCR Purification kits (Qiagen) for sequencing.</p><p>For differentiation of CCoV subgenotypes, primers 1bF, 5′-TTG ATT CAA AGA TTT GAG TAT
TGG-3′ and CCVSR, 5′-GTT AGT TTG TCT AAT AAT ACC AAC ACC-3′, were used to amplify the
5′-terminal region of the S gene [<xref rid="r30" ref-type="bibr">30</xref>]. RT-PCR was
performed using a TaKaRa RNA LA PCR <sup>TM</sup> kit (AMV) Ver.1.1 (Takara, Otsu, Japan).
RT was carried out with random 9-mer primers at 30°C for 10 min, 42°C for 30 min and 99°C
for 5 min, and then, PCR was performed. Amplified fragments were purified using a QIAquick
PCR Purification kit (Qiagen) for sequencing.</p></sec><sec><title>Virus isolation</title><p><italic>Felis catus</italic> whole fetus-4 cells (fcwf-4 cells; ATCC Number: CRL-2787)
[<xref rid="r11" ref-type="bibr">11</xref>] were maintained in Dulbecco’s minimum
essential medium (DMEM; Life Technologies, St. Louis, MO, U.S.A.) containing 10%
heat-inactivated fetal calf serum (FCS; Sigma-Aldrich), 100 units/m<italic>l</italic>penicillin and 100 <italic>µ</italic>g/m<italic>l</italic> streptomycin (Life
Technologies). Fcwf-4 cells in 6-well plates were inoculated with extracts from
CCoV-positive feces and were then incubated at 37°C in a 5% CO<sub>2</sub> incubator.
Cells were observed daily for cytopathic effects (CPE). If there were no CPE, cells were
blind-passaged five times.</p></sec><sec><title>Plaque-purification</title><p>Isolated CCoV was plaque-purified three times. Briefly, 10 PFU of CCoV were inoculated on
fcwf-4 cells in 6-well plates. After 1 hr of adsorption, inoculum was removed, and 0.8%
agarose in DMEM containing 10% FCS was overlaid on cells. After the appearance of CPE,
plaques were picked up by tips and dissolved into DMEM. This plaque-purification procedure
was repeated three times.</p></sec><sec><title>Nucleotide sequence analysis</title><p>The sequence of the 3′-terminal one-third of the viral genome from S gene to poly A was
determined by RT-PCR using TaKaRa RNA LA PCR<sup>TM</sup> kit (AMV) Ver.1.1 (Takara). RT
was carried out with random 9-mer primers at 30°C for 10 min, 42°C for 30 min, 99°C for 5
min and 4°C or oligo dT-Adaptor primer at 42°C for 30 min, 99°C for 5 min and 4°C for 5
min. Then, PCR was performed with the following primers: 1bF, 5′-TTG ATT CAA AGA TTT GAG
TAT TGG-3′; CCVSR, 5′-GTT AGT TTG TCT AAT AAT ACC AAC ACC-3′; CCVScenF, 5′-TAA GTA ACA TCA
CAC TAC C-3′; S6, 5′-CCA AGG CCA TTT TAC ATA AG-3′; ScenFF3, 5′-CTG GAC TGT ACC TGA ATT
G-3′; and the reverse primer M13 primer M4, 5′-GTT TTC CCA GTC ACG AC-3′.</p><p>In order to amplify the S gene of CCoV-IIa, PCR was performed using the following pimers:
1bF, CCVSR, CCVS2CenF, 5′- CTA TTC TGT GAC ACC ATG TG-3′ [<xref rid="r30" ref-type="bibr">30</xref>] and 2bR. Amplified products were confirmed by electrophoresis on 0.8%
agarose gels and were then purified using the QIAquick PCR Purification kit (Qiagen). The
nucleotide sequences were determined by an ABI PRISM 310 Genetic Analyzer auto sequencer
(Applied Biosystems, Carlsbad, CA, U.S.A.). Sequences were assembled and analyzed using
GENETYX<sup>®</sup> ver.8 (Software Development Co., Tokyo, Japan).</p></sec><sec><title>Virus-neutralizing (VN) test</title><p>VN testing was performed using fcwf-4 cells as described previously [<xref rid="r26" ref-type="bibr">26</xref>, <xref rid="r30" ref-type="bibr">30</xref>] with
modifications. CCoV-IIa fc1, isolated in Japan in 1990 [<xref rid="r1" ref-type="bibr">1</xref>], and CCoV-IIb CCoV/dog/HCM47/2015 strain, which was isolated and
plaque-purified three times in this study, were used. Briefly, dog sera were inactivated
at 56°C for 30 min before VN test. Equal volumes of two-fold serially diluted sera and
virus solution containing 2.0 × 10<sup>3</sup> PFU/m<italic>l</italic> of CCoV were mixed
and incubated at 37°C for 1 hr. Then, 50 <italic>µl</italic> of this mixture was
inoculated onto fcwf-4 cells monolayer in 24-well plates. After adsorption at 37°C for 1
hr, inoculum was removed, and 0.8% agarose (Lonza, Rockland, ME, U.S.A.) in DMEM
containing 10% FCS was overlaid. Infected cells were incubated at 37°C until CPE was
observed, followed by fixing with phosphate-buffered formalin and staining with crystal
violet. When the number of plaques was less than 75% of those in control wells, diluted
sera were judged to be positive. Titers were expressed as the highest serum dilution
showing 75% plaque reduction or more.</p></sec><sec><title>Phylogenetic analysis</title><p>Phylogenetic relationships based on the nucleotide sequences of the 5′-terminal region of
S genes or complete S genes were analyzed using distance-based (neighbor-joining) with
MEGA 7.0 software [<xref rid="r13" ref-type="bibr">13</xref>]. Bootstrap values were
calculated based on 1,000 replicates.</p></sec><sec><title>Statistical analysis</title><p>Chi-squared and Fisher’s exact probability tests were used for statistical analysis.
<italic>P</italic> values of <0.05 were considered to be statistically
significant.</p></sec></sec><sec sec-type="results" id="s2"><title>RESULTS</title><sec><title>Prevalence of antibody against CCoV-II in dogs in Ho Chi Minh</title><p>Eighty-seven dogs (43.3%) were positive for anti-CCoV-II antibody. Prevalence of
anti-CCoV-II antibody in dogs aged over 3 years (52.0%) was significantly higher than that
in dogs aged under 1 year (28.6%) (<italic>P</italic><<italic>0.05</italic>).
Prevalence of anti-CCoV-II antibody in Vietnamese (39.2%) was significantly lower than
that in other breeds (63.3%) (<xref rid="tbl_001" ref-type="table">Table
1</xref><table-wrap id="tbl_001" orientation="portrait" position="float"><label>Table 1.</label><caption><title>Prevalence of anti-CCoV-II antibody among 201 domestic dogs in Ho Chi Minh
City, Vietnam</title></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="2" align="left" rowspan="1"></th><th align="center" rowspan="1" colspan="1">No. of examined dogs</th><th align="center" rowspan="1" colspan="1">No. of positive dogs</th><th align="center" rowspan="1" colspan="1">Ratio of positive dogs (%)</th></tr></thead><tbody><tr><td rowspan="2" align="left" colspan="1">Sex</td><td align="left" rowspan="1" colspan="1">Female</td><td align="center" rowspan="1" colspan="1">101</td><td align="center" rowspan="1" colspan="1">45</td><td align="center" rowspan="1" colspan="1">44.6</td></tr><tr><td align="left" rowspan="1" colspan="1">Male</td><td align="center" rowspan="1" colspan="1">100</td><td align="center" rowspan="1" colspan="1">42</td><td align="center" rowspan="1" colspan="1">42.0</td></tr><tr><td colspan="4" rowspan="1"><hr></hr></td></tr><tr><td rowspan="4" align="left" colspan="1">Age</td><td align="left" rowspan="1" colspan="1"><1</td><td align="center" rowspan="1" colspan="1">28</td><td align="center" rowspan="1" colspan="1">8</td><td align="center" rowspan="1" colspan="1">28.6<sup>a)</sup></td></tr><tr><td align="left" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">44</td><td align="center" rowspan="1" colspan="1">14</td><td align="center" rowspan="1" colspan="1">31.8</td></tr><tr><td align="left" rowspan="1" colspan="1">2</td><td align="center" rowspan="1" colspan="1">54</td><td align="center" rowspan="1" colspan="1">26</td><td align="center" rowspan="1" colspan="1">48.1</td></tr><tr><td align="left" rowspan="1" colspan="1">≥3</td><td align="center" rowspan="1" colspan="1">75</td><td align="center" rowspan="1" colspan="1">39</td><td align="center" rowspan="1" colspan="1">52.0<sup>a)</sup></td></tr><tr><td colspan="4" rowspan="1"><hr></hr></td></tr><tr><td rowspan="3" align="left" colspan="1">Breed</td><td align="left" rowspan="1" colspan="1">Vietnamese</td><td align="center" rowspan="1" colspan="1">120</td><td align="center" rowspan="1" colspan="1">47</td><td align="center" rowspan="1" colspan="1">39.2<sup>b)</sup></td></tr><tr><td align="left" rowspan="1" colspan="1">Mixed</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">21</td><td align="center" rowspan="1" colspan="1">41.2</td></tr><tr><td align="left" rowspan="1" colspan="1">Other</td><td align="center" rowspan="1" colspan="1">30</td><td align="center" rowspan="1" colspan="1">19</td><td align="center" rowspan="1" colspan="1">63.3<sup>b)</sup></td></tr><tr><td colspan="4" rowspan="1"><hr></hr></td></tr><tr><td colspan="2" align="left" rowspan="1">Total</td><td align="center" rowspan="1" colspan="1">201</td><td align="center" rowspan="1" colspan="1">87</td><td align="center" rowspan="1" colspan="1">43.3</td></tr></tbody></table><table-wrap-foot><p>a, b) Significant difference (<italic>P</italic><0.05).</p></table-wrap-foot></table-wrap>). Antibody titer against CCoV-II ranged from 1:10 to 1:320 (data not
shown).</p></sec><sec><title>Detection of CCoV in diarrheic and healthy dogs</title><p>To detect CCoV-I and CCoV-II genes in fecal samples, RT-PCR was carried out using fecal
samples from 30 diarrheic and 50 healthy dogs. Although CCoV-I was not detected, CCoV-II
was detected from two diarrheic dogs (6.7%) and five healthy dogs (10%, 5/50) (<xref ref-type="supplementary-material" rid="pdf_001">Table S1</xref>).
Next, nucleotide sequences of 5′-terminal region of the S gene were analyzed to
differentiate subgenotypes of CCoV-II and were deposited into the DNA database of Japan
(DDBJ; Accession No. LC190901-LC190907) (<xref ref-type="supplementary-material" rid="pdf_001">Table S1</xref>). Phylogenetic analysis based on the
5′-terminal region of the S gene showed that one and six strains belonged to CCoV-IIa and
CCoV-IIb, respectively <bold>(</bold><xref ref-type="fig" rid="fig_001">Fig. 1</xref><fig orientation="portrait" fig-type="figure" id="fig_001" position="float"><label>Fig. 1.</label><caption><p>Phylogenetic analysis based on 5′-terminal region of spike genes (476 nt).
Vietnamese CCoVs in feces collected from diarrheic and healthy dogs are shown in
bold. GeneBank accession numbers of reference strains are as follows: CCoV-II: SK378
(KC175341), K378 (KC175340), Insavc-1 (D13096.1), BGF10 (AY342160.1), NA/09
(JF682842.1), CB/05 (KP981644.1), fc1 (AB781790), TN449 (JQ404410), 171 (KC175339),
Chinese ferret CoV/DM95/2003 (EF192156.1), NTU-336 (GQ477367), 430/07 (EU924790),
174/06 (EU856362), 341/05 (EU856361.1), 66/09 (HQ450376), 68/09 (HQ450377.1), 119/08
(EU924791.1) and Raccoon dog CoV/GZ43/2003 (EF192155). FCoV-I: UU20 (HQ392471.1),
UU31 (HQ012371.1) and Yayoi (AB695067.1); FCoV-II: NTU156 (GQ152141.1), DF-2
(DQ286398.1), M91-267 (AB781788.1) and Tokyo/cat/130627 (AB907624.1<bold>)</bold>.
CCoV-I: 23/03 (KP84972.1) and Elmo/02 (AY307020.1); TGEV<bold>:</bold> Purdue
(DQ811789.2) and TS (DQ201447).</p></caption><graphic xlink:href="jvms-79-343-g001"></graphic></fig> and <xref ref-type="supplementary-material" rid="pdf_001">Table S1</xref>). Vietnamese CCoVs-IIb formed one cluster and was similar to Chinese
ferret badger DM95/2003 (95.4–95.6%) and CCoV/NTU336/F/2008 (95.2–95.6%). Vietnamese
CCoV-IIa was similar to Raccoon dog GZ43/2003 (95.6%) (<xref ref-type="fig" rid="fig_001">Fig. 1</xref>).</p></sec><sec><title>Phylogenetic analysis based on S genes</title><p>Next, the full length of the S gene of CCoV/dog/HCM27/2014 was also determined (4,362 nt,
DDBJ Accession No. LC190906). Phylogenetic analysis based on complete S genes showed that
Vietnamese CCoV/HCM47/2015 was similar to Chinese ferret badger CoV/DM95/2003 (95.9%) and
CCoV/NTU336/F/2008 (95.2%), and that Vietnamese CCoV-IIa, CCoV/dog/HCM27/2014 was similar
to Raccoon dog CoV/GZ43/2003 (97.4%) (<xref ref-type="fig" rid="fig_002">Fig. 2</xref><fig orientation="portrait" fig-type="figure" id="fig_002" position="float"><label>Fig. 2.</label><caption><p>Phylogenetic analysis based on full length of S gene of CCoV. Vietnamese isolated
and detected CCoV strains are shown in bold. GeneBank accession numbers of reference
strains are as follows: CCoV-II: SK378 (KC175341), K378 (KC175340), Insavc-1
(D13096.1), BGF10 (AY342160.1), NA/09 (JF682842.1), CB/05 (KP981644.1), fc1
(AB781790), TN449 (JQ404410), 171 (KC175339), DM95/2003 (EF192156.1), NTU-336
(GQ477367), 430/07 (EU924790), 174/06 (EU856362), 341/05 (EU856361.1), 66/09
(HQ450376), 68/09 (HQ450377.1), 119/08 (EU924791.1) and Raccoon dog CoV/GZ43/2003
(EF192155). FCoV-I: UU20 (HQ392471.1), UU31 (HQ012371.1) and Yayoi (AB695067.1).
FCoV-II: NTU156 (GQ152141.1), DF-2 (DQ286398.1), M91-267 (AB781788.1) and
Tokyo/cat/130627 (AB907624.1). CCoV-I: 23/03 (KP84972.1) and Elmo/02 (AY307020.1);
TGEV<bold>:</bold> Purdue (DQ811789.2) and TS (DQ201447).</p></caption><graphic xlink:href="jvms-79-343-g002"></graphic></fig>).</p></sec><sec><title>Virus isolation and large deletion in plaque-purified CCoV</title><p>One CCoV-IIb was successfully isolated from a healthy dog (female, six years old) and
designated as CCoV/dog/HCM47/2015. For further analysis, the isolate was plaque-purified
three times, and the nucleotide sequence of the 3′-terminal one-third CCoV genome from the
S gene to poly A (8,995 nt) was determined. Surprisingly, the plaque-purified CCoV had a
large deletion in the ORF3abc and partial E genes (1,165 nt), and a short deletion in the
ORF7b gene (60 nt). Next, we determined nucleotide sequences of the original virus in the
feces, confirming that the original virus in feces did not have any deletions (DDBJ
Accession No. LC190907) (<xref ref-type="fig" rid="fig_003">Fig. 3</xref><fig orientation="portrait" fig-type="figure" id="fig_003" position="float"><label>Fig. 3.</label><caption><p>Schema of 3′-terminal one-third of CCoV/dog/HCM47/2015. Nucleotides sequences of
CCoV/dog/HCM47/2015 in fecal sample (A) and plaque-purified virus (B) were analyzed.
Plaque-purified CCoV has a large deletion in ORF3abc and partial E genes (1,165 nt),
and a small deletion in the ORF7b gene (60 nt) in comparison with the original CCoV
in fecal samples.</p></caption><graphic xlink:href="jvms-79-343-g003"></graphic></fig>).</p></sec><sec><title>Comparison of antinenicity between CcoV-IIa and -IIb</title><p>To compare antibody titers against CCoV-IIa and -IIb, 60 sera were examined by VN testing
using fc1 and plaque-purified CCoV/dog/HCM47/2015, respectively. The results showed that
positivity of antibody against CCoV-IIb (58.3%) was slightly higher than that against
CCoV-IIa (51.7%) (<xref rid="tbl_002" ref-type="table">Table 2</xref><table-wrap id="tbl_002" orientation="portrait" position="float"><label>Table 2.</label><caption><title>Comparison of VN antibodies against CCoV-IIa fc1 and CCoV-IIb
CCoV/dog/HCM47/2015 among 60 domestic dogs in Ho Chi Minh City, Vietnam</title></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="2" rowspan="3" align="left"></th><th colspan="2" align="center" valign="middle" rowspan="1">VN test against CCoV/dog/HCM47/2015</th><th rowspan="3" align="center" valign="middle" colspan="1">Total</th></tr><tr><th colspan="2" rowspan="1"><hr></hr></th></tr><tr><th align="center" rowspan="1" colspan="1">Positive</th><th align="center" rowspan="1" colspan="1">Negative</th></tr></thead><tbody><tr><td rowspan="2" align="left" colspan="1">VN test against fc1</td><td align="left" rowspan="1" colspan="1">Positive</td><td align="center" rowspan="1" colspan="1">31</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">31 (51.7%)</td></tr><tr><td align="left" rowspan="1" colspan="1">Negative</td><td align="center" rowspan="1" colspan="1">4</td><td align="center" rowspan="1" colspan="1">25</td><td align="center" rowspan="1" colspan="1">29 (48.3%)</td></tr><tr><td colspan="4" rowspan="1"><hr></hr></td></tr><tr><td colspan="2" align="left" rowspan="1">Total</td><td align="center" rowspan="1" colspan="1">35 (58.3%)</td><td align="center" rowspan="1" colspan="1">25 (41.7%)</td><td align="center" rowspan="1" colspan="1">60 (100.0%)</td></tr></tbody></table></table-wrap>). Four additional dogs became positive for anti-CCoV-IIb antibody, and nine
dogs had significantly higher antibody titers (over 4-fold) against CCoV-IIb than CCoV-IIa
(data not shown).</p></sec></sec><sec sec-type="discussion" id="s3"><title>DISCUSSION</title><p>In this study, the prevalence of anti-CCoV-II anibody was 43.3%, suggesting that CCoV-II
has been spreading among the dog population in Ho Chi Minh, Vietnam. Seroprevalance of CCoV
infection was 15.8% in the open population and 40.8% in kenneled populations in Australia,
44.1% in Japan, 90.8% in Italy and 96.5% in Turkey [<xref rid="r1" ref-type="bibr">1</xref>,
<xref rid="r9" ref-type="bibr">9</xref>, <xref rid="r19" ref-type="bibr">19</xref>, <xref rid="r24" ref-type="bibr">24</xref>]. Sera from dogs in Vietnam reacted more strongly with
CCoV-IIb than CCoV-IIa (<xref rid="tbl_002" ref-type="table">Table 2</xref>), indicating
that CCoV-IIb is the major genotype in Vietnam. The results of RT-PCR in this study also
supported the notion that CCoV-IIb is the predominant genotype circulating in domestic dogs
in Vietnam (<xref ref-type="fig" rid="fig_001">Fig.1</xref>, <xref ref-type="supplementary-material" rid="pdf_001">Table S1</xref>).</p><p>The prevalance of antibody against CCoV-II increased with age (<xref rid="tbl_001" ref-type="table">Table 1</xref>). Similar results were reported in Turkey [<xref rid="r9" ref-type="bibr">9</xref>]. Older dogs must have more opportunities to be infected
with CCoV. Seroprevalence of CCoV-II in imported breeds (63.3%) was significantly higher
than that in domestic breeds (39.2%). There have been similar reports in Japan [<xref rid="r27" ref-type="bibr">27</xref>, <xref rid="r29" ref-type="bibr">29</xref>],
indicating that many dogs are infected with CCoV while housed with breeders or in pet
shops.</p><p>In this study, two diarrheic dogs (6.7%) and five healthy dogs (10%) were positive for
CCoV-II, but no dogs were positive for CCoV-I. One of seven Vietnamese CCoVs strains was
positive for CCoV-IIa, and others were positive for CCoV-IIb. Positivity for CCoV-I and
CCoV-II in feces of dogs has been reported in Japan (CCoV-I: 53.2% and CCoV-II: 56.9%)
[<xref rid="r28" ref-type="bibr">28</xref>], China (CCoV-I: 4.5% and CCoV-II: 23.9%)
[<xref rid="r32" ref-type="bibr">32</xref>], Italy (CCoV-I: 25.2% and CCoV-II: 36.3%),
United Kingdom (CCoV-I: 15.0% and CCoV-II: 20.6%), Hungary (CCoV-I: 22% and CCoV-II: 15%),
Greece (CCoV-I: 37% and CCoV-II: 36%) [<xref rid="r7" ref-type="bibr">7</xref>], Brazil
(CCoV-I: 47% and CCoV-II: 63%) [<xref rid="r5" ref-type="bibr">5</xref>] and Korea (CCoV-I:
22% and CCoV-II: 10%) [<xref rid="r12" ref-type="bibr">12</xref>]. In Vietnam, CCoV-II,
especially CCoV-IIb, may be more predominant among the dog population than CCoV-I. However,
CCoV-I infection in Vietnamese dogs should be examined by RT-PCR using further primer sets
specific for CCoV-I.</p><p>Both CCoV-IIa and IIb cause enteritis, and the lesion is limited to the small intestine
[<xref rid="r17" ref-type="bibr">17</xref>]. On the other hand, pantropic CCoV-IIa spread
systemically and caused hemorrhagic gastroenteritis, neurological signs and leukopenia
[<xref rid="r8" ref-type="bibr">8</xref>, <xref rid="r16" ref-type="bibr">16</xref>].
CCoV-IIb also spread systemically and infected to internal organs, when it co-infected with
canine parvovirus [<xref rid="r16" ref-type="bibr">16</xref>, <xref rid="r21" ref-type="bibr">21</xref>]. However, there were no significant differences in CCoV infection
between diarrheic dogs and healthy dogs. CCoV infection may not be a serious problem in
Vietnamese dogs. Further studies will be required to clarify the pathogenicity of CCoV in
Vietnam.</p><p>Phylogenetic and sequence analysis based on S genes showed that Vietnamese CCoV-IIa
(CCoV/dog/HCM27/2014) and CCoV-IIb (CCoV/dog/HCM47/2015) were smilar to CCoVs in China,
Chinese ferret badger CoV/DM95/2003 and raccoon dog CoV/GZ43/2003, respectively (<xref ref-type="fig" rid="fig_002">Fig.2</xref><bold>)</bold>. These Chinese CoVs were found in
live animal markets in Shenzhen and Guangzhou, Guangdong Province, China [<xref rid="r31" ref-type="bibr">31</xref>], suggesting that Vietnamese CCoVs might have the same
ancestor as these Chinese CCoVs. In our previous study, canine distemper virus in Vietnam
was also similar to Chinese viruses [<xref rid="r20" ref-type="bibr">20</xref>].</p><p>We succeeded in isolation of CCoV/dog/HCM47/2015 and plague-purified the isolate three
times for further characterization. Surprisingly, the plaque-purified CCoV had a large
deletion in the ORF3abc and partial E genes (1,165 nt) and a short deletion of ORF7b (60 nt)
(<xref ref-type="fig" rid="fig_003">Fig. 3</xref>). Deletions in ORF3a (47 nt) and ORF3b
(31 nt) in CCoV 1–71 [<xref rid="r18" ref-type="bibr">18</xref>], a deletion in ORF3b (38
nt) in CB/05 [<xref rid="r8" ref-type="bibr">8</xref>] and a deletion in ORF7b (154 nt) in
341/05 [<xref rid="r7" ref-type="bibr">7</xref>] have also been reported. These data
indicate that ORF3abc and ORF7b are not essential and that they are stable in viral
replication <italic>in vitro</italic>, but not <italic>in vivo</italic>. In feline CoV, it
was reported that ORF3abc plays an important role in the efficient macrophage and monocyte
tropism [<xref rid="r2" ref-type="bibr">2</xref>] and that deletion of ORF7b is correlated
with a loss of virulence [<xref rid="r10" ref-type="bibr">10</xref>]. In our preliminary
data, two dogs orally inoculated with plaque-purified CCoV/dog/HCM47/2015 did not show any
clinical signs, but anti-CCoV antibody increased after challenge. Now, we are examining the
virulence of this plaque-purified CCoV. Importantly, virus isolation is important for
characterization, but rapid adaptation by passage of coronaviruses should be monitored.</p><p>In conclusion, this is the first characterization of CCoV in Vietnam. In Vietnam, CCoV-IIa
and CCoV-IIb, but not CCoV-I, are co-circulating among domestic dogs. This plaque-purified
CCoV/dog/HCM47/2015 may be a good tool for diagnosis of CCoV infection, because of its rapid
viral growth <italic>in vitro</italic> and antigenicity. Furthermore, the virus is a
candidate for inactivated and/or attenuated live vaccines, because genetic markers in
ORF3abc and 7b are able to differentiate it from field isolates.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="pdf_001"><caption><title>Supplement table</title></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jvms-79-343-s001.pdf" orientation="portrait" xlink:type="simple" id="d35e802" position="anchor"></media></supplementary-material></sec></body><back><ack><p>We would like to thank the veterinarians at animal hospitals for sample
collection. This study was funded by the Japan Society for the Promotion and Science (JSPS)
KAKENHI (Grant No. 15H04599) and the Japan Agency for Medical Research and Development
(AMED). The authors would like to acknowledge the technical expertise of The DNA Core
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