Skip to main content
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2008 Jun 12;80(8):1441–1446. doi: 10.1002/jmv.21218

Study of influenza C virus infection in France

S Gouarin 1,, A Vabret 1, J Dina 1, J Petitjean 1, J Brouard 2, D Cuvillon‐Nimal 2, F Freymuth 1
PMCID: PMC7166557  PMID: 18551600

Abstract

From November 2004 to April 2007, specimens were obtained from 2,281 patients with acute respiratory tract illness in Normandy, France. Eighteen strains of influenza C virus were detected in these samples using a combined tissue culture/RT‐PCR diagnostic method. Most patients with influenza C virus infection (13/18) were infants or young children (<2 years of age). The most frequent symptoms were fever and cough, and the clinical presentation of influenza C virus infection was similar to that of other respiratory viruses. Thirteen of the 18 infected patients were hospitalized; 3 presented with a severe lower respiratory infection. The hemagglutinin‐esterase (HE) gene of 10 isolates was sequenced to determine the lineages of the circulating influenza C viruses. Phylogenetic analysis revealed that most of the isolated strains had an HE gene belonging to the C/Yamagata/26/81‐related lineage. These results show that influenza C virus regularly circulates in Normandy and generally causes a mild upper respiratory infection. Because the differential clinical diagnosis of influenza C virus infection is not always easy, it is important to identify viral strains for both patient management and epidemiological purposes. J. Med. Virol. 80:1441–1446, 2008. © 2008 Wiley‐Liss, Inc.

Keywords: respiratory infection, multiplex RT‐PCR assay, phylogenetic analysis

REFERENCES

  1. Adachi K, Kitame F, Sugawara K, Nishimura H, Nakamura K. 1989. Antigenic and genetic characterization of three influenza C strains isolated in the Kinki district of Japan in 1982‐1983. Virology 172: 125–133. [DOI] [PubMed] [Google Scholar]
  2. Bellau‐Pujol S, Vabret A, Legrand L, Dina J, Gouarin S, Petitjean‐Lecherbonnier J, Pozzetto B, Ginevra C, Freymuth F. 2005. Development of three multiplex RT‐PCR assays for the detection of 12 respiratory RNA viruses. J Virol Methods 126: 53–63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buonagurio DA, Nakada S, Desselberger U, Krystal M, Palese P. 1985. Non cumulative sequence changes in the hemagglutinin genes of influenza C virus isolates. Virology 146: 221–232. [DOI] [PubMed] [Google Scholar]
  4. Calvo C, Garcia‐Garcia ML, Centeno M, Perez‐Brena P, Casas I. 2006. Influenza C virus infection in children, Spain. Emerg Infect Dis 12: 1621–1622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Claas ECJ, Sprenger MJW, Kleter GEM, van Beek R, Quint WGV, Masurel N. 1992. Type‐specific identification of influenza A, B, and C by the polymerase chain reaction. J Virol Methods 39: 1–13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coiras MT, Perez‐Brena P, Garcia ML, Casas I. 2003. Simultaneous detection of influenza A, B, and C viruses, respiratory syncytial virus, and adenoviruses in clinical samples by multiplex reverse transcription nested‐PCR assay. J Med Virol 69: 132–144. [DOI] [PubMed] [Google Scholar]
  7. Dykes AC, Cherry JC, Nolan CE. 1980. A clinical, epidemiologic, serologic and virologic study of Influenza C virus infection. Arch Intern Med 140: 1295–1298. [PubMed] [Google Scholar]
  8. Eugene‐Ruellan G, Freymuth F, Bahloul C, Bradane H, Vabret A, Tordo N. 1998. Detection of respiratory syncytial virus A and B and parainfluenza virus 3 sequences in respiratory tracts of infants by a single PCR with primers targeted to the L‐polymerase gene and differential hybridization. J Clin Microbiol 36: 796–801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Freymuth F, Vabret A, Rozenberg F, Dina J, Petitjean J, Gouarin S, Corbet S, Brouard J, Lebon P. 2005. Replication of respiratory viruses, particularly influenza virus, rhinovirus and coronavirus in HuH7 hepatocarcinoma cell line. J Med Virol 77: 295–301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galtier N, Gouy M, Gautier C. 1996. SeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543–548. [DOI] [PubMed] [Google Scholar]
  11. Greenbaum E, Morag A, Zakay‐Rones Z. 1998. Isolation of influenza C virus during an outbreak on influenza A and B viruses. J Clin Microbiol 36: 1441–1442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Guittet V, Brouard J, Vabret A, Lafay F, Guillois B, Duhamel JF, Freymuth F. 2003. Rhinovirus and accurate respiratory infections in hospitalized children. Retrospective study 1998‐2000. Arch Pediatr 10: 417–423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirsila M, Kauppila J, Tuomaala K, Grekula B, Puhakka T, Ruuskanen O, Ziegler T. 2001. Detection by reverse transcription‐polymerase chain reaction of influenza C in nasopharyngeal secretions of adults with common cold. J Infect Dis 183: 1269–1272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Homma M, Ohyama S, Katagiri S. 1982. Age distribution of the antibody to type C influenza virus. Microbiol Immunol 27: 639–642. [DOI] [PubMed] [Google Scholar]
  15. Jartti T, Lehtinen P, Vuorinen T, Koskenvuo M, Ruuskanen O. 2004. Persistence of rhinovirus and enterovirus RNA after acute respiratory illness in children. J Med Virol 72: 695–699. [DOI] [PubMed] [Google Scholar]
  16. Katagiri S, Ohizumi A, Homma M. 1983. An outbreak of type C influenza in a children's home. J Infect Dis 148: 51–56. [DOI] [PubMed] [Google Scholar]
  17. Kimura H, Abiko C, Peng G, Muraki Y, Sugawara K, Hongo S, Kitame F, Mizuta K, Numazaki Y, Suzuki H, Nakamura K. 1997. Interspecies transmission of influenza C virus between humans and pigs. Virus Res 48: 71–79. [DOI] [PubMed] [Google Scholar]
  18. Manuguerra JC, Hannoun C, Aymard M. 1992. Influenza C virus infection in France. J Infect 24: 91–99. [DOI] [PubMed] [Google Scholar]
  19. Matsuzaki Y, Muraki Y, Sugawara K, Hongo S, Nishimura H, Kitame F, Katsushima N, Numazaki Y, Nakamura K. 1994. Cocirculation of two distinct groups of influenza C virus in Yamagata city, Japan. Virology 202: 796–802. [DOI] [PubMed] [Google Scholar]
  20. Matsuzaki Y, Mizuta K, Kimura K, Sugawara K, Ttsuchiya E, Suzuki H, Hongo S, Nakamura K. 2000. Characterization of antigenically unique influenza C virus strains isolated in Yamagata and Sendai cities, Japan, during 1992‐1993. J Gen Virol 81: 1447–1452. [DOI] [PubMed] [Google Scholar]
  21. Matsuzaki Y, Sugawara K, Mizuta K, Tsuchiya E, Muraki Y, Hongo S, Suzuki H, Nakamura K. 2002. Antigenic and genetic characterization of influenza C viruses which caused two outbreaks in Yamagata City, Japan, in 1996 and 1998. J Clin Microbiol 40: 422–429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matsuzaki Y, Mizuta K, Sugawara K, Tsuchiya E, Muraki Y, Hongo S, Suzuki H, Nishimura H. 2003. Frequent reassortment among Influenza C viruses. J Virol 77: 871–881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Matsuzaki Y, Katsushima N, Nagai Y, Makoto S, Tsutomu I, Michiyo S, Setsuko K, Katsumi M, Nishimura H. 2006. Clinical features of influenza C virus infection in children. J Infect Dis 193: 1229–1235. [DOI] [PubMed] [Google Scholar]
  24. Matsuzaki Y, Abiko C, Mizuta K, Sugawara K, Takashita E, Muraki Y, Suzuki H, Mikawa M, Shimada S, Sato K, Kuzuya M, Takao S, Wakatsuki K, Itagaki T, Hongo S, Nishimura H. 2007. A nationwide epidemic of influenza C virus infection in Japan in 2004. J Clin Microbiol 45: 783–788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moriuchi H, Katsushima N, Nishimura H, Nakamura K, Numazaki Y. 1991. Community‐acquired influenza C virus infection in children. J Pediatr 118: 235–238. [DOI] [PubMed] [Google Scholar]
  26. Muraki Y, Hongo S, Sugawara K, Kitame F, Nakamura K. 1996. Evolution of the hemagglutinin‐esterase gene of influenza C virus. J Gen Virol 77: 673–679. [DOI] [PubMed] [Google Scholar]
  27. Muraki Y, Washioka H, Sugawara K, Matsuzaki Y, Takashita E, Hongo S. 2004. Identification of an amino acid residue on influenza C virus M1 protein responsible for formation of the cord‐like structures of the virus. J Gen Virol 85: 1885–1893. [DOI] [PubMed] [Google Scholar]
  28. Nishimura H, Sugawara K, Kitame F, Nakamura K, Sasaki H. 1987. Prevalence of the antibody to influenza C virus in a northern Luzon Highland village, Phillippines. Microbiol Immunol 31: 1137–1143. [DOI] [PubMed] [Google Scholar]
  29. O'Callaghan RJ, Gohd RS, Labat DD. 1980. Human antibody to influenza C virus: Its age‐related distribution and distinction from receptor analogs. Infect Immun 30: 500–505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sugawara K, Nishimura H, Kitame F, Nakamura K. 1986. Antigenic variation among human strains of influenza C virus detected with monoclonal antibodies to gp88 glycoprotein. Virus Res 6: 27–32. [DOI] [PubMed] [Google Scholar]
  31. Templeton KE, Scheltinga SA, Beersma MF, Kroes AC, Claas EC. 2004. Rapid and sensitive method using multiplex real‐time PCR for diagnosis of infections by influenza A and B viruses, respiratory syncytial virus, and parainfluenza viruses 1, 2, 3,and 4. J Clin Microbiol 42: 1564–1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vabret A, Dina J, Gouarin S, Petitjean J, Corbet S, Freymuth F. 2006. Detection of the new coronavirus HK U1:a report of 6 cases. Clin Infect Dis 42: 634–639. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Medical Virology are provided here courtesy of Wiley

RESOURCES