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Influenza D Virus of New Phylogenetic Lineage, Japan

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Influenza D Virus of New Phylogenetic Lineage, Japan RESEARCH LETTERS of death were higher for patients with multiple and Influenza D Virus of New more severe underlying conditions. Further studies are necessary to better clarify the mechanisms that Phylogenetic Lineage, Japan lead to severe outcomes among these patients. For case-patients infected with MERS-CoV, the Shin Murakami, Ryota Sato, Hiroho Ishida, presence and compounding of underlying condi- Misa Katayama, Akiko Takenaka-Uema, tions, including DM, hypertension, and, ultimately, Taisuke Horimoto COD, corresponded with an increasingly complicated clinical course and death. These findings indicate that Author affiliations: University of Tokyo, Tokyo, Japan increased clinical vigilance is warranted for patients (S. Murakami, H. Ishida, M. Katayama, A. Takenaka-Uema, with multiple and severe underlying conditions who T. Horimoto); Yamagata Livestock Hygiene Service Center, are suspected of being infected with MERS-CoV. Yamagata, Japan (R. Sato) DOI: https://doi.org/10.3201/eid2601.191092 About the Author Influenza D virus (IDV) can potentially cause respiratory Dr. Alanazi is director general of infection prevention and diseases in livestock. We isolated a new IDV strain from control at the Ministry of Health, Riyadh, Saudi Arabia. diseased cattle in Japan; this strain is phylogenetically His research interests include prevention and control of and antigenically distinguished from the previously de- infectious diseases in the healthcare setting. scribed IDVs. nfluenza D virus (IDV; family Orthomyxoviridae) is References 1. World Health Organization. Regional office for the Eastern Ione of the possible bovine respiratory disease com- Mediterranean. MERS situation update; October 2018 [cited plex (BRDC) causative agents. IDVs are detected in and 2019 Oct 30]. http://www.emro.who.int/pandemic- isolated from cattle in many countries in North Amer- epidemic-diseases/mers-cov/mers-situation-update- ica, Asia, Europe, and Africa (1–4). In addition, both october-2018.html 2. Assiri A, Al-Tawfiq JA, Al-Rabeeah AA, Al-Rabiah FA, IDV RNAs and specific antibodies have been detected Al-Hajjar S, Al-Barrak A, et al. Epidemiological, in many animal species (1,5,6). To date, IDVs have demographic, and clinical characteristics of 47 cases of been phylogenetically classified into 3 lineages: D/OK, Middle East respiratory syndrome coronavirus disease D/660, and Japanese lineages. We isolated a new IDV from Saudi Arabia: a descriptive study. Lancet Infect Dis. 2013;13:752–61. https://doi.org/10.1016/ strain from cattle in Japan with respiratory disease, S1473-3099(13)70204-4 whose hemagglutinin-esterase-fusion (HEF) gene did 3. Alqahtani FY, Aleanizy FS, Ali El Hadi Mohamed R, not belong to the known phylogenetical lineages. Alanazi MS, Mohamed N, Alrasheed MM, et al. Prevalence At a herd in Yamagata Prefecture in northern Ja- of comorbidities in cases of Middle East respiratory syndrome coronavirus: a retrospective study. Epidemiol pan, 15 Holsteins (37.5% of bred cattle in the herd) Infect. 2018;Nov 5:1–5. had respiratory signs develop during January 6–10, 4. Al-Abdely HM, Midgley CM, Alkhamis AM, Abedi GR, 2019 (Appendix Table 1, http://wwwnc.cdc.gov/ Lu X, Binder AM, et al. Middle East respiratory syndrome EID/article/26/1/19-1092-App1.pdf). We collected coronavirus infection dynamics and antibody responses among clinically diverse patients, Saudi Arabia. Emerg nasal swab samples from 9 of 15 cows on January 7 Infect Dis. 2019;25:753–66. https://doi.org/10.3201/ and 10. All samples subjected to IDV-specific real- eid2504.181595 time reverse transcription PCR (RT-PCR) (7) were 5. Alraddadi BM, Watson JT, Almarashi A, Abedi GR, found positive. We also subjected these samples to Turkistani A, Sadran M, et al. Risk factors for primary Middle East respiratory syndrome coronavirus illness in RT-PCR analyses specific for bovine viral diarrhea humans, Saudi Arabia, 2014. Emerg Infect Dis. 2016;22:49–55. virus 1 and 2, infectious bovine rhinotracheitis vi- https://doi.org/10.3201/eid2201.151340 rus, bovine parainfluenza virus 3, bovine respiratory syncytial virus, bovine coronavirus, bovine rhinitis A Address for correspondence: Glen R. Abedi, Centers for Disease virus, Mycobacterium bovis, Mycoplasma bovigenitalium, Control and Prevention, 1600 Clifton RD NE, Mailstop A34, Mycoplasma dispar, Ureaplasma diversum, and Myco- Atlanta, GA 30329-4027, USA; email: [email protected] plasma bovirhinis. All samples were found negative for these pathogens except for the sample from cow no. 5, which was positive for M. dispar. Despite these cows receiving antimicrobial drug treatment, we isolated Mannheimia haemolytica from 7 of them (nos. 1–5, 7, 8); cow no. 5 died on January 7. Taken together, these 168 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 1, January 2020 RESEARCH LETTERS Figure. Phylogenetic trees for the 7 nucleotide genomic segments of D/bovine/Yamagata/1/2019 (arrow), an influenza D virus of a new phylogenetic lineage, Japan. A) Polymerase basic protein 2; B) polymerase basic protein 1; C) polymerase protein 3; D) hemagglutinin-esterase-fusion protein; E) nucleoprotein; F) matrix protein; and G) nonstructural protein segments. Maximum- likelihood analysis, in combination with 500 bootstrap replicates, was used to derive trees based on nucleotide sequences of the genomic segments. Bootstrap values are shown above and to the left of the major nodes. Scale bars indicate nucleotide substitutions per site. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 1, January 2020 169 RESEARCH LETTERS factors suggested that IDV infection was involved in Oklahoma/1334/2011 (D/OK) in the D/OK-lin- the onset of BRDC in this herd. eage (1), D/bovine/Nebraska/9–5/2012 (D/NE) To isolate IDV, we inoculated the collected sam- in the D/660-lineage (9), and D/bovine/Yamaga- ples into human rectal tumor HRT-18G cells (Ameri- ta/10710/2016 (D/Yama2016) in the Japanese lin- can Type Culture Collection [ATCC] no. CRL-11663), eage (10), by performing HI tests using anti-IDV incubated the cells for 4 days at 37°C, and blindly pas- mouse serum and a panel of anti-HEF monoclonal saged the supernatants in swine testis ST cells (ATCC antibodies (Appendix Table 2). We observed 1-way no. CRL-1746) in the presence of tosyl phenylalanyl cross-reactivity between D/Yama2019 and D/OK or chloromethyl ketone-treated trypsin. We observed a D/Yama2016 with antiserum. Monoclonal antibody cytopathic effect at the second passage. For further clones B4 and R36 cross-reacted to D/Yama2019 and analysis, we used supernatants that tested positive other tested viruses with different titers, whereas the for hemagglutination (HA) and for presence of IDV clones G22, G27, and G74, which reacted strongly to RNA detected by real-time RT-PCR, indicating suc- D/Yama2016, did not react to D/Yama2019. These cessful isolation of IDV (designated as D/bovine/ data indicated HEF antigenic heterogeneity between Yamagata/1/2019 [D/Yama2019]). We determined D/Yama2019 and viruses of the 3 known lineages. the entire genomic sequence of D/Yama2019 by per- Monoclonal antibodies revealed the presence of com- forming RT-PCR amplification of each viral segment mon epitopes among IDVs, as suggested by previous with specific primers, revealing an identical sequence reports (9,10). Amino acid differences were located with that detected in swab sample no. 1. We depos- on the head region of HEF among the IDVs, possibly ited our sequence data in GenBank (accession nos. causing antigenic heterogeneity. LC494105–11). In summary, we isolated a newly identified We phylogenetically analyzed the sequences of IDV from diseased cattle that was phylogeneti- D/Yama2019 by performing maximum-likelihood cally and antigenically distinguished from known analysis using MEGA version X (8). The HEF se- IDVs. Further epidemiologic studies are needed to quence of D/Yama2019 acquired an independent clarify invasion and epidemic status of these heter- position different from that exhibited in any other ologous IDVs, but our results indicated that heter- lineage, whereas those of the other segments were ologous IDVs are circulating in close vicinity within positioned relatively close to the preexisting Japa- the prefecture. nese strains, in which polymerase basic protein 1 and 2, polymerase protein 3, nucleoprotein, and Acknowledgments nonstructural protein sequences were of the Japa- We thank Ben M. Hause for the viruses used in the study. nese lineage, whereas the matrix sequence was of the D/OK lineage (Figure). S.M. is supported by a Grant-in-Aid for the Encouragement We also collected serum samples from 8 cows on of Young Scientists (A) (grant no. 17H05042). T.H. is January 10 (acute phase of the disease) and February supported by Livestock Promotion Funds from the Japan 4 (recovery phase) and examined them for antibod- Racing Association. ies against D/Yama2019 by using the HA inhibi- tion (HI) test (Appendix Table 1). We treated serum About the Author samples with receptor-destroying enzyme (RDEII; Denka Seiken, Tokyo, Japan, https://www.denka. Dr. Murakami is an associate professor at the Graduate co.jp) before the HI test, which was done with the D/ School of Agricultural and Life Sciences, University Yama2019 antigen and 0.6% turkey erythrocyte sus- of Tokyo, Tokyo, Japan. His research interests include pension. We considered samples with HI titer >1:40 epidemiologic and molecular biological studies of animal to be positive (4). All serum samples collected on Jan- viruses, including influenza viruses. uary 7 were HI-negative except for the sample from cow no. 1 (a titer of 1:40), whereas all samples col- References lected on February 4 were HI-positive (a titer range 1. Hause BM, Ducatez M, Collin EA, Ran Z, Liu R, Sheng Z, of 1:40–1:160), confirming seroconversion to IDV anti- et al. Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human bodies in diseased cows.
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