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Surveillance Open Access
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Abstract

Introduction

Recent data on influenza C virus indicate a possible higher clinical impact in specified patient populations than previously thought.

Aim

We aimed to investigate influenza C virus circulation in Germany.

Methods

A total of 1,588 samples from 0 to 4 year-old children presenting as outpatients with influenza-like illness (ILI) or acute respiratory infection were analysed retrospectively. The samples represented a subset of all samples from the German national surveillance system for influenza in this age group in 2012–14. The presence of influenza C virus was investigated by real-time PCR. For positive samples, information on symptoms as well as other respiratory virus co-infections was considered. Retrieved influenza C viral sequences were phylogenetically characterised.

Results

Influenza C viral RNA was detected in 20 (1.3% of) samples, including 16 during the 2012/13 season. The majority (18/20) of influenza C-positive patients had ILI according to the European Union definition, one patient had pneumonia. Viruses belonged to the C/Sao Paulo and C/Kanagawa lineages. Most (11/20) samples were co-infected with other respiratory viruses.

Conclusion

Our data are the first on influenza C virus circulation in Germany and notably from a European national surveillance system. The low detection frequency and the identified virus variants confirm earlier observations outside a surveillance system. More virus detections during the 2012/13 season indicate a variable circulation intensity in the different years studied. Influenza C virus can be considered for ILI patients. Future studies addressing its clinical impact, especially in patients with severe disease are needed.

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/content/10.2807/1560-7917.ES.2019.24.10.1800174
2019-03-07
2024-12-20
/content/10.2807/1560-7917.ES.2019.24.10.1800174
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References

  1. World Health Organisation (WHO). Influenza (Seasonal) Fact sheet. Geneva: WHO; November 2016. Available from: http://www.who.int/mediacentre/factsheets/fs211/en/
  2. Joosting AC, Head B, Bynoe ML, Tyrrell DA. Production of common colds in human volunteers by influenza C virus. BMJ. 1968;4(5624):153-4.  https://doi.org/10.1136/bmj.4.5624.153  PMID: 5681050 
  3. Kauppila J, Rönkkö E, Juvonen R, Saukkoriipi A, Saikku P, Bloigu A, et al. Influenza C virus infection in military recruits--symptoms and clinical manifestation. J Med Virol. 2014;86(5):879-85.  https://doi.org/10.1002/jmv.23756  PMID: 24122799 
  4. Calvo C, García-García ML, Borrell B, Pozo F, Casas I. Prospective study of influenza C in hospitalized children. Pediatr Infect Dis J. 2013;32(8):916-9.  https://doi.org/10.1097/INF.0b013e31828fca10  PMID: 23624431 
  5. Shimizu Y, Abiko C, Ikeda T, Mizuta K, Matsuzaki Y. Influenza C Virus and Human Metapneumovirus Infections in Hospitalized Children With Lower Respiratory Tract Illness. Pediatr Infect Dis J. 2015;34(11):1273-5.  https://doi.org/10.1097/INF.0000000000000863  PMID: 26244834 
  6. Matsuzaki Y, Katsushima N, Nagai Y, Shoji M, Itagaki T, Sakamoto M, et al. Clinical features of influenza C virus infection in children. J Infect Dis. 2006;193(9):1229-35.  https://doi.org/10.1086/502973  PMID: 16586359 
  7. Moriuchi H, Katsushima N, Nishimura H, Nakamura K, Numazaki Y. Community-acquired influenza C virus infection in children. J Pediatr. 1991;118(2):235-8.  https://doi.org/10.1016/S0022-3476(05)80489-5  PMID: 1993950 
  8. Odagiri T, Matsuzaki Y, Okamoto M, Suzuki A, Saito M, Tamaki R, et al. Isolation and characterization of influenza C viruses in the Philippines and Japan. J Clin Microbiol. 2015;53(3):847-58.  https://doi.org/10.1128/JCM.02628-14  PMID: 25552361 
  9. Principi N, Scala A, Daleno C, Esposito S. Influenza C virus–associated community-acquired pneumonia in children. Influenza Other Respir Viruses. 2013;7(6):999-1003.  https://doi.org/10.1111/irv.12062  PMID: 23594251 
  10. Gouarin S, Vabret A, Dina J, Petitjean J, Brouard J, Cuvillon-Nimal D, et al. Study of influenza C virus infection in France. J Med Virol. 2008;80(8):1441-6.  https://doi.org/10.1002/jmv.21218  PMID: 18551600 
  11. Matsuzaki Y, Sugawara K, Abiko C, Ikeda T, Aoki Y, Mizuta K, et al. Epidemiological information regarding the periodic epidemics of influenza C virus in Japan (1996-2013) and the seroprevalence of antibodies to different antigenic groups. J Clin Virol. 2014;61(1):87-93.  https://doi.org/10.1016/j.jcv.2014.06.017  PMID: 25017953 
  12. Arbeitsgemeinschaft Influenza. Bericht zur Epidemiologie der Influenza in Deutschland Saison 2015/16; 2016. German.
  13. European Commission. Commission Implementing Decision (EU) 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions; 2018. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=uriserv:OJ.L_.2018.170.01.0001.01.ENG
  14. Schulze M, Nitsche A, Schweiger B, Biere B. Diagnostic approach for the differentiation of the pandemic influenza A(H1N1)v virus from recent human influenza viruses by real-time PCR. PLoS One. 2010;5(4):e9966.  https://doi.org/10.1371/journal.pone.0009966  PMID: 20376359 
  15. Matsuzaki Y, Ikeda T, Abiko C, Aoki Y, Mizuta K, Shimotai Y, et al. Detection and quantification of influenza C virus in pediatric respiratory specimens by real-time PCR and comparison with infectious viral counts. J Clin Virol. 2012;54(2):130-4.  https://doi.org/10.1016/j.jcv.2012.02.012  PMID: 22398038 
  16. Nakada S, Creager RS, Krystal M, Aaronson RP, Palese P. Influenza C virus hemagglutinin: comparison with influenza A and B virus hemagglutinins. J Virol. 1984;50(1):118-24. PMID: 6699942 
  17. Atkinson KV, Bishop LA, Rhodes G, Salez N, McEwan NR, Hegarty MJ, et al. Influenza C in Lancaster, UK, in the winter of 2014-2015. Sci Rep. 2017;7(1):46578.  https://doi.org/10.1038/srep46578  PMID: 28406194 
  18. Homma M, Ohyama S, Katagiri S. Age distribution of the antibody to type C influenza virus. Microbiol Immunol. 1982;26(7):639-42.  https://doi.org/10.1111/mim.1982.26.7.639  PMID: 7132793 
  19. Pabbaraju K, Wong S, Wong A, May-Hadford J, Tellier R, Fonseca K. Detection of influenza C virus by a real-time RT-PCR assay. Influenza Other Respir Viruses. 2013;7(6):954-60.  https://doi.org/10.1111/irv.12099  PMID: 23445084 
  20. Racaniello VR, Palese P. Isolation of influenza C virus recombinants. J Virol. 1979;32(3):1006-14. PMID: 513198 
  21. Antón A, Marcos MA, Codoñer FM, de Molina P, Martínez A, Cardeñosa N, et al. Influenza C virus surveillance during the first influenza A (H1N1) 2009 pandemic wave in Catalonia, Spain. Diagn Microbiol Infect Dis. 2011;69(4):419-27.  https://doi.org/10.1016/j.diagmicrobio.2010.11.006  PMID: 21396539 
  22. Howard LM, Johnson M, Gil AI, Pekosz A, Griffin MR, Edwards KM, et al. , RESPIRA-PERU Group. A novel real-time RT-PCR assay for influenza C tested in Peruvian children. J Clin Virol. 2017;96:12-6.  https://doi.org/10.1016/j.jcv.2017.08.014  PMID: 28917132 
  23. Manuguerra JC, Hannoun C, Aymard M. Influenza C virus infection in France. J Infect. 1992;24(1):91-9.  https://doi.org/10.1016/0163-4453(92)91150-A  PMID: 1312564 
  24. Smith DB, Gaunt ER, Digard P, Templeton K, Simmonds P. Detection of influenza C virus but not influenza D virus in Scottish respiratory samples. J Clin Virol. 2016;74:50-3.  https://doi.org/10.1016/j.jcv.2015.11.036  PMID: 26655269 
  25. Hirsilä M, Kauppila J, Tuomaala K, Grekula B, Puhakka T, Ruuskanen O, et al. Detection by reverse transcription-polymerase chain reaction of influenza C in nasopharyngeal secretions of adults with a common cold. J Infect Dis. 2001;183(8):1269-72.  https://doi.org/10.1086/319675  PMID: 11262210 
  26. Akinloye OM, Rönkkö E, Savolainen-Kopra C, Ziegler T, Iwalokun BA, Deji-Agboola MA, et al. Specific viruses detected in nigerian children in association with acute respiratory disease. J Trop Med. 2011;2011:690286.  https://doi.org/10.1155/2011/690286  PMID: 22007241 
  27. Jelley L, Levy A, Deng YM, Spirason N, Lang J, Buettner I, et al. Influenza C infections in Western Australia and Victoria from 2008 to 2014. Influenza Other Respir Viruses. 2016;10(6):455-61.  https://doi.org/10.1111/irv.12402  PMID: 27373693 
  28. Nesmith N, Williams JV, Johnson M, Zhu Y, Griffin M, Talbot HK. Sensitive Diagnostics Confirm That Influenza C is an Uncommon Cause of Medically Attended Respiratory Illness in Adults. Clin Infect Dis. 2017;65(6):1037-9.  https://doi.org/10.1093/cid/cix471  PMID: 28541414 
  29. Johnson G, Nour AA, Nolan T, Huggett J, Bustin S. Minimum information necessary for quantitative real-time PCR experiments. Methods Mol Biol. 2014;1160:5-17.  https://doi.org/10.1007/978-1-4939-0733-5_2  PMID: 24740217 
  30. Matsuzaki Y, Sugawara K, Furuse Y, Shimotai Y, Hongo S, Oshitani H, et al. Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014. J Virol. 2016;90(18):8251-65.  https://doi.org/10.1128/JVI.00969-16  PMID: 27384661 
  31. Reiche J, Jacobsen S, Neubauer K, Hafemann S, Nitsche A, Milde J, et al. Human metapneumovirus: insights from a ten-year molecular and epidemiological analysis in Germany. PLoS One. 2014;9(2):e88342.  https://doi.org/10.1371/journal.pone.0088342  PMID: 24505479 
  32. Reiche J, Schweiger B. Genetic variability of group A human respiratory syncytial virus strains circulating in Germany from 1998 to 2007. J Clin Microbiol. 2009;47(6):1800-10.  https://doi.org/10.1128/JCM.02286-08  PMID: 19386848 
  33. Wang M, Veit M. Hemagglutinin-esterase-fusion (HEF) protein of influenza C virus. Protein Cell. 2016;7(1):28-45.  https://doi.org/10.1007/s13238-015-0193-x  PMID: 26215728 
  34. Furuse Y, Matsuzaki Y, Nishimura H, Oshitani H. Analyses of Evolutionary Characteristics of the Hemagglutinin-Esterase Gene of Influenza C Virus during a Period of 68 Years Reveals Evolutionary Patterns Different from Influenza A and B Viruses. Viruses. 2016;8(12):321.  https://doi.org/10.3390/v8120321  PMID: 27898037 
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