Antiviral Susceptibilities of Distinct Lineages of Influenza C and D Viruses

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2023 Jan 21

PMID 36680284

Authors

Emi Takashita

Shin Murakami

Yoko Matsuzaki

Seiichiro Fujisaki

Hiroko Morita

Shiho Nagata

Misa Katayama

Katsumi Mizuta

Hidekazu Nishimura

Shinji Watanabe

Taisuke Horimoto

Hideki Hasegawa

Affiliations

Soon will be listed here.

Abstract

The emergence and spread of antiviral-resistant influenza viruses are of great concern. To minimize the public health risk, it is important to monitor antiviral susceptibilities of influenza viruses. Analyses of the antiviral susceptibilities of influenza A and B viruses have been conducted globally; however, those of influenza C and D viruses are limited. Here, we determined the susceptibilities of influenza C viruses representing all six lineages (C/Taylor, C/Yamagata, C/Sao Paulo, C/Aichi, C/Kanagawa, and C/Mississippi) and influenza D viruses representing four lineages (D/OK, D/660, D/Yama2016, and D/Yama2019) to RNA polymerase inhibitors (baloxavir and favipiravir) by using a focus reduction assay. All viruses tested were susceptible to both drugs. We then performed a genetic analysis to check for amino acid substitutions associated with baloxavir and favipiravir resistance and found that none of the viruses tested possessed these substitutions. Use of the focus reduction assay with the genotypic assay has proven valuable for monitoring the antiviral susceptibilities of influenza C and D viruses as well as influenza A and B viruses. Antiviral susceptibility monitoring of all influenza virus types should continue in order to assess the public health risks posed by these viruses.

Citing Articles

Baloxavir Resistance Markers in Influenza A and B Viruses in the Americas.

Acocal-Juarez E, Marquez-Dominguez L, Vallejo-Ruiz V, Cedillo L, Santos-Lopez G Drug Healthc Patient Saf. 2024; 16:105-113.

PMID: 39296541 PMC: 11410037. DOI: 10.2147/DHPS.S470868.

Monitoring Influenza C and D Viruses in Patients With Respiratory Diseases in Japan, January 2018 to March 2023.

Shimizu K, Kawakami C, Matsuzaki Y, Fujisaki S, Nagata S, Morita H Influenza Other Respir Viruses. 2024; 18(6):e13345.

PMID: 38923307 PMC: 11196370. DOI: 10.1111/irv.13345.

Influenza C virus susceptibility to antivirals with different mechanisms of action.

Chesnokov A, Ivashchenko A, Matsuzaki Y, Takashita E, Mishin V, Ivachtchenko A Antimicrob Agents Chemother. 2024; 68(5):e0172723.

PMID: 38587392 PMC: 11064526. DOI: 10.1128/aac.01727-23.

Total Osteopontin and Its Isoform OPN4 Are Differently Expressed in Respiratory Samples during Influenza A(H1N1)pdm09 Infection and Progression.

Martins J, Sousa T, Oliveira M, Gimba E, Siqueira M, da Rocha Matos A Microorganisms. 2023; 11(5).

PMID: 37317323 PMC: 10224194. DOI: 10.3390/microorganisms11051349.

References

Hause B, Ducatez M, Collin E, Ran Z, Liu R, Sheng Z . Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses. PLoS Pathog. 2013; 9(2):e1003176. PMC: 3567177. DOI: 10.1371/journal.ppat.1003176. View

Thielen B, Friedlander H, Bistodeau S, Shu B, Lynch B, Martin K . Detection of Influenza C Viruses Among Outpatients and Patients Hospitalized for Severe Acute Respiratory Infection, Minnesota, 2013-2016. Clin Infect Dis. 2017; 66(7):1092-1098. PMC: 5862734. DOI: 10.1093/cid/cix931. View

Takashita E, Kinoshita N, Yamayoshi S, Sakai-Tagawa Y, Fujisaki S, Ito M . Efficacy of Antibodies and Antiviral Drugs against Covid-19 Omicron Variant. N Engl J Med. 2022; 386(10):995-998. PMC: 8809508. DOI: 10.1056/NEJMc2119407. View

Takashita E, Kawakami C, Morita H, Ogawa R, Fujisaki S, Shirakura M . Detection of influenza A(H3N2) viruses exhibiting reduced susceptibility to the novel cap-dependent endonuclease inhibitor baloxavir in Japan, December 2018. Euro Surveill. 2019; 24(3). PMC: 6344841. DOI: 10.2807/1560-7917.ES.2019.24.3.1800698. View

Murakami S, Sato R, Ishida H, Katayama M, Takenaka-Uema A, Horimoto T . Influenza D Virus of New Phylogenetic Lineage, Japan. Emerg Infect Dis. 2019; 26(1):168-171. PMC: 6924913. DOI: 10.3201/eid2601.191092. View

Peng Q, Liu Y, Peng R, Wang M, Yang W, Song H . Structural insight into RNA synthesis by influenza D polymerase. Nat Microbiol. 2019; 4(10):1750-1759. DOI: 10.1038/s41564-019-0487-5. View

Takashita E, Ichikawa M, Morita H, Ogawa R, Fujisaki S, Shirakura M . Human-to-Human Transmission of Influenza A(H3N2) Virus with Reduced Susceptibility to Baloxavir, Japan, February 2019. Emerg Infect Dis. 2019; 25(11):2108-2111. PMC: 6810216. DOI: 10.3201/eid2511.190757. View

Odagiri T, Matsuzaki Y, Okamoto M, Suzuki A, Saito M, Tamaki R . Isolation and characterization of influenza C viruses in the Philippines and Japan. J Clin Microbiol. 2015; 53(3):847-58. PMC: 4390655. DOI: 10.1128/JCM.02628-14. View

Taylor R . Studies on survival of influenza virus between epidemics and antigenic variants of the virus. Am J Public Health Nations Health. 1949; 39(2):171-8. PMC: 1527782. DOI: 10.2105/ajph.39.2.171. View

10.

Bailey E, Choi J, Zemke J, Yondon M, Gray G . Molecular surveillance of respiratory viruses with bioaerosol sampling in an airport. Trop Dis Travel Med Vaccines. 2018; 4:11. PMC: 6142699. DOI: 10.1186/s40794-018-0071-7. View

11.

Takada K, Kawakami C, Fan S, Chiba S, Zhong G, Gu C . A humanized MDCK cell line for the efficient isolation and propagation of human influenza viruses. Nat Microbiol. 2019; 4(8):1268-1273. DOI: 10.1038/s41564-019-0433-6. View

12.

Uehara T, Hayden F, Kawaguchi K, Omoto S, Hurt A, de Jong M . Treatment-Emergent Influenza Variant Viruses With Reduced Baloxavir Susceptibility: Impact on Clinical and Virologic Outcomes in Uncomplicated Influenza. J Infect Dis. 2019; 221(3):346-355. DOI: 10.1093/infdis/jiz244. View

13.

Takashita E, Kawakami C, Ogawa R, Morita H, Fujisaki S, Shirakura M . Influenza A(H3N2) virus exhibiting reduced susceptibility to baloxavir due to a polymerase acidic subunit I38T substitution detected from a hospitalised child without prior baloxavir treatment, Japan, January 2019. Euro Surveill. 2019; 24(12). PMC: 6440584. DOI: 10.2807/1560-7917.ES.2019.24.12.1900170. View

14.

Govorkova E, Takashita E, Daniels R, Fujisaki S, Presser L, Patel M . Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2018-2020. Antiviral Res. 2022; 200:105281. PMC: 9254721. DOI: 10.1016/j.antiviral.2022.105281. View

15.

Asha K, Kumar B . Emerging Influenza D Virus Threat: What We Know so Far!. J Clin Med. 2019; 8(2). PMC: 6406440. DOI: 10.3390/jcm8020192. View

16.

Takashita E, Morita H, Ogawa R, Nakamura K, Fujisaki S, Shirakura M . Susceptibility of Influenza Viruses to the Novel Cap-Dependent Endonuclease Inhibitor Baloxavir Marboxil. Front Microbiol. 2018; 9:3026. PMC: 6291754. DOI: 10.3389/fmicb.2018.03026. View

17.

Zhai S, Zhang H, Chen S, Zhou X, Lin T, Liu R . Influenza D Virus in Animal Species in Guangdong Province, Southern China. Emerg Infect Dis. 2017; 23(8):1392-1396. PMC: 5547803. DOI: 10.3201/eid2308.170059. View

18.

Mishin V, Patel M, Chesnokov A, La Cruz J, Nguyen H, Lollis L . Susceptibility of Influenza A, B, C, and D Viruses to Baloxavir. Emerg Infect Dis. 2019; 25(10):1969-1972. PMC: 6759234. DOI: 10.3201/eid2510.190607. View

19.

Hirotsu N, Sakaguchi H, Sato C, Ishibashi T, Baba K, Omoto S . Baloxavir Marboxil in Japanese Pediatric Patients With Influenza: Safety and Clinical and Virologic Outcomes. Clin Infect Dis. 2019; 71(4):971-981. PMC: 7428393. DOI: 10.1093/cid/ciz908. View

20.

Horimoto T, Hiono T, Mekata H, Odagiri T, Lei Z, Kobayashi T . Nationwide Distribution of Bovine Influenza D Virus Infection in Japan. PLoS One. 2016; 11(9):e0163828. PMC: 5040247. DOI: 10.1371/journal.pone.0163828. View