Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Archives of Virology
Published in: Archives of Virology 1/2020

01-01-2020 | Influenza | Original Article

Displacement of the Gent/1999 human-like swine H1N2 influenza A virus lineage by novel H1N2 reassortants in Germany

Authors: Roland Zell, Marco Groth, Andi Krumbholz, Jeannette Lange, Anja Philipps, Ralf Dürrwald

Published in: Archives of Virology | Issue 1/2020

Login to get access

Abstract

A swine influenza survey was conducted between 2003 and 2015 in Germany. During this period, 8122 snout swabs or other respiratory specimens from pigs of 5178 herds, mainly from Germany, were investigated for the presence of swine influenza A virus (S-IAV). In total, 1310 S-IAV isolates were collected. Of this collection, the complete genome of 267 H1N2 S-IAV isolates was sequenced and phylogenetically analyzed. The data demonstrate the incursion of human-like swine H1N2 viruses (Gent/1999-like) in 2000 and prevalent circulation until 2010. From 2008 onward, a sustained and broad change of the genetic constellation of the swine H1N2 subtype commenced. The Gent/1999-like swine H1N2 viruses ceased and several new swine H1N2 reassortants emerged and became prevalent in Germany. Of these, the upsurge of the Diepholz/2008-like, Emmelsbuell/2009-like and Papenburg/2010-like viruses is notable. The data reveal the importance of reassortment events in S-IAV evolution. The strong circulation of S-IAV of different lineages in the swine population throughout the year underlines that pigs are important reservoir hosts.
Appendix
Available only for authorised users
Literature
1.
McCauley JW, Hongo S, Kaverin NV, Kochs G, Lanb RA, Matrosovich MN, Perez DR, Palese P, Presti RM, Rimstad E, Smith GJD (2012) Family Orthomyxoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Amsterdam, pp 749–761
2.
Zell R, Scholtissek C, Ludwig S (2013) Genetics, evolution, and the zoonotic capacity of European swine influenza viruses. Curr Top Microbiol Immunol 370:29–55PubMed
3.
Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF (2014) Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22:183–191PubMedPubMedCentral
4.
Webster RG, Bean WJ, Gorman WT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56(1):152–179PubMedPubMedCentral
5.
Lu G, Rowley T, Garten R, Donis RO (2007) FluGenome: a web tool for genotyping influenza A virus. Nucl Acids Res 35:W275–W279PubMedPubMedCentral
6.
Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon KJ, Krauss S, Webster RG (1999) Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73:8851–8856PubMedPubMedCentral
7.
Olsen CW (2002) The emergence of novel swine influenza viruses in North America. Virus Res 85:199–210PubMed
8.
Brown IH, Harris PA, McCauley JW, Alexander DJ (1998) Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J Gen Virol 79:2947–2955PubMed
9.
Van Reeth K, Brown IH, Pensaert M (2000) Isolations of H1N2 influenza A virus from pigs in Belgium. Vet Rec 146:588–589PubMed
10.
Schrader C, Suss J (2003) Genetic characterization of a porcine H1N2 influenza virus strain isolated in Germany. Intervirology 46:66–70PubMed
11.
Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Foucher RAM, Pappas C, Alpuche-Aranda CM, Lopez-Gatell H, Olivera H, Lopez I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD Jr, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, Donis R, Katz J, Finelli L, Bridges CB, Shaw M, Jernigan DB, Uyeki TM, Smith DJ, Klimov AI, Cox N (2009) Antigenic and genetic characterization of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201PubMedPubMedCentral
12.
Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JSM, Guan Y, Rambaut A (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122–1125PubMed
13.
Moreno A, Di Trani L, Alborali L, Vaccari G, Barbieri I, Falcone E, Sozzi E, Puzelli S, Ferri G, Cordioli P (2010) First pandemic H1N1 outbreak from a pig farm in Italy. Open Virol J 4:52–56PubMedPubMedCentral
14.
Vijaykrishna D, Poon LLM, Zhu HC, Ma SK, Li OTW, Cheung CL, Smith GJD, Peiris JSM, Guan Y (2010) Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328:1529PubMedPubMedCentral
15.
Welsh MD, Baird PM, Guelbenzu-Gonzalo MP, Hanna A, Reid SM, Essen S, Russell C, Thomas S, Barrass L, McNeilly F, McKillen J, Todd D, Harkin V, McDowell S, Choudhury B, Irvine RM, Borobia J, Grant J, Brown IH (2010) Initial incursion of pandemic (H1N1) 2009 influenza A virus into European pigs. Vet Rec 166:642–645PubMed
16.
Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ (2011) Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629PubMedPubMedCentral
17.
Hoen SC, Strugnell BW, Russell C, Barrass L, Reid SM, Brown IH (2011) Reassortant pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg Infect Dis 17(6):1049–1052
18.
Moreno A, Di Trani L, Faccini S, Vaccari G, Nigrelli D, Boniotti MB, Falcone E, Boni A, Chiapponi C, Sozzi E, Cordioli P (2011) Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 149:472–477PubMed
19.
Starick E, Lange E, Fereidouni S, Bunzenthal C, Höveler R, Kuczka A, Grosse Beilage E, Hamann HP, Klingelhöfer I, Steinhauer D, Vahlenkamp T, Beer M, Harder T (2011) Reassorted pandemic (H1N1) 2009 influenza A viruses discovered from pigs in Germany. J Gen Virol 92:1184–1188PubMed
20.
Liang H, Lam TTY, Fan X, Chen X, Zeng Y, Zhou J, Duan L, Tse M, Chan CH, Li L, Leung TY, Yip CH, Cheung CL, Zhou B, Smith DK, Poon LLM, Peiris M, Guan Y, Zhu H (2014) Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. J Virol 88:19864–19874
21.
Lange J, Groth M, Schlegel M, Krumbholz A, Wieczorek K, Ulrich R, Köppen S, Schulz K, Appl D, Selbitz HJ, Sauerbrei A, Platzer M, Zell R, Dürrwald R (2013) Reassortment of the pandemic (H1N1) 2009 virus and establishment of a novel porcine H1N2 influenza virus lineage in Germany. Vet Microbiol 167:345–356PubMed
22.
Zell R, Bergmann S, Krumbholz A, Wutzler P, Dürrwald R (2008) Ongoing evolution of swine influenza viruses: a novel reassortant. Arch Virol 153:2085–2092PubMed
23.
Zell R, Motzke S, Krumbholz A, Wutzler P, Herwig V, Dürrwald R (2008) Novel reassortant of swine influenza H1N2 virus in Germany. J Gen Virol 89:271–276PubMed
24.
Krumbholz A, Schmidtke M, Bergmann S, Motzke S, Bauer K, Stech J, Dürrwald R, Wutzler P, Zell R (2009) High prevalence of amantadine resistance among circulating European porcine influenza A viruses. J Gen Virol 90:900–908PubMed
25.
Lange J, Groth M, Kanrai P, Pleschka S, Scholtissek C, Dürrwald R, Platzer M, Sauerbrei A, Zell R (2014) Circulation of classical swine influenza virus in Europe between the wars? Arch Virol 159:1467–1473PubMed
26.
Stech J, Stech O, Herwig A, Altmeppen H, Hundt J, Gohrbandt S, Kreibich A, Weber S, Klenk HD, Mettenleiter TC (2008) Rapid and reliable universal cloning of influenza A virus genes by target-primed plasmid amplification. Nucl Acids Res 36:e139PubMedPubMedCentral
27.
Groth M, Lange J, Kanrai P, Pleschka S, Scholtissek C, Krumbholz A, Platzer M, Sauerbrei A, Zell R (2014) The genome of an influenza virus from a pilot whale: Relation to influenza viruses of gulls and marine mammals. Infect Genet Evol 24:183–186PubMed
28.
Tamura K, Peterson D, Peterson N (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedPubMedCentral
29.
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMed
30.
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUTi and the BEAST 1.7. Mol Biol Evol 29:1969–1973PubMedPubMedCentral
31.
Rozas J, Sanches-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMed
32.
Anderson TK, Macken CA, Lewis NS, Scheuermann RH, Van Reeth K, Brown IH, Swenson SL, Simon G, Saito T, Berhane Y, Ciacci-Zanella J, Pereda A, Davis CT, Donis RO, Webby RJ, Vincent AL (2016) A phylogeny-based global nomenclature system and automated annotation tool for H1 hemagglutinin genes from swine influenza A viruses. mSphere 1(6):e00275–16PubMedPubMedCentral
33.
Watson SJ, Langat P, Reid SM, Lam TTY, Cotten M, Kelly M, Van Reeth K, Qiu Y, Simon G, Bonin E, Foni E, Chiapponi C, Larsen L, Hjulsager C, Markowska-Daniel I, Urbaniak K, Dürrwald R, Schlegel M, Huovilainen A, Davidson I, Dan A, Loeffen W, Edwards S, Bublot M, Vila T, Maldonado J, Valls L, ESNIP3 Consortium, Brown IH, Pybus OG, Kellam P (2015) Molecular epidemiology and evolution of influenza viruses circulating within European swine between 2009 and 2013. J Virol 89(19):9920–9931PubMedPubMedCentral
34.
Moreno A, Chiapponi C, Boniotti MB, Sozzi E, Foni E, Barbieri I, Zanoni MG, Faccini S, Lelli D, Cordioli P (2012) Genomic characterization of H1N2 swine influenza viruses in Italy. Vet Microbiol 156(3–4):265–276PubMed
35.
Campitelli L, Donatelli I, Foni E, Castrucci MR, Fabiani C, Kawaoka Y, Krauss S, Webster RG (1997) Continued evolution of H1N1 and H3N2 influenza viruses in pigs in Italy. Virology 232:310–318PubMed
36.
Harder TC, Grosse Beilage E, Lange E, Meiners C, Döhring S, Pesch S, Noe T, Grund C, Beer M, Starick E (2013) Expanded cocirculation of stable subtypes, emerging lineages, and new sporadic reassortants of porcine influenza viruses in swine populations in Northwest Germany. J Virol 87(19):10460–10476PubMedPubMedCentral
37.
Krumbholz A, Philipps A, Oehring H, Schwarzer K, Eitner A, Wutzler P, Zell R (2011) Current knowledge on PB1-F2 of influenza A viruses. Med Microbiol Immunol 200:69–75PubMed
38.
Bálint A, Metreveli G, Widén F, Zohari S, Berg M, Isaksson M, Renström LH, Wallgren P, Belák S, Segall T, Kiss I (2009) The first Swedish H1N2 swine influenza virus isolate represents an uncommon reassortant. Virol J 6:180PubMedPubMedCentral
39.
Metreveli G, Emmoth E, Zohari S, Bálint A, Widén F, Muradrasoli S, Wallgren P, Belák S, Leblanc N, Berg M, Kiss I (2011) Comparison of two H1N2 swine influenza A viruses from disease outbreaks in pigs in Sweden during 2009 and 2010. Virus Genes 42(2):236–244PubMed
40.
Brown IH (2013) History and epidemiology of swine influenza in Europe. Curr Top Microbiol Immunol 370:133–146PubMed
41.
Bhatt S, Lam TT, Lycett SJ, Leigh Brown AJ, Bowden TA, Holmes EC, Guan Y, Wood JLN, Brown IH, Kellam P, Combating Swine Influenza Consortium, Pybus OG (2013) The evolutionary dynamics of influenza A virus adaptation to mammalian hosts. Phil Trans R Soc B 368:20120382PubMedPubMedCentral
42.
Bedford T, Riley S, Barr IG, Broor S, Chadha M, Cox NJ, Daniels RS, Gunasekaran CP, Hurt AC, Kelso A, Klimov A, Lewis NS, Li Y, McCauley JW, Odagiri T, Potdar V, Rambaut A, Shu Y, Skepner E, Smith DJ, Suchard MA, Tashiro M, Wang D, Xu X, Lemey P, Russell CA (2015) Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature 523:217–220PubMedPubMedCentral
43.
Lyons DM, Lauring AS (2018) Mutation and epistasis in influenza virus evolution. Viruses 10:407PubMedCentral
44.
Krumbholz A, Lange J, Dürrwald R, Walther M, Müller TH, Kühnel D, Wutzler P, Sauerbrei A, Zell R (2014) Prevalence of antibodies to European porcine influenza viruses in humans living in high pig density areas of Germany. Med Microbiol Immunol 203(1):13–24PubMed
Metadata
Title
Displacement of the Gent/1999 human-like swine H1N2 influenza A virus lineage by novel H1N2 reassortants in Germany
Authors
Roland Zell
Marco Groth
Andi Krumbholz
Jeannette Lange
Anja Philipps
Ralf Dürrwald
Publication date
01-01-2020
Publisher
Springer Vienna
Keyword
Influenza
Published in
Archives of Virology / Issue 1/2020
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-019-04457-w

Other articles of this Issue 1/2020

Archives of Virology 1/2020 Go to the issue

Original Article

Characterization and genome sequencing of a novel T7-like lytic phage, kpssk3, infecting carbapenem-resistant Klebsiella pneumoniae

Annotated Sequence Record

Complete genome sequence of a novel capillovirus infecting Hevea brasiliensis in China

Annotated Sequence Record

Complete genomic sequence of tea-oil camellia deltapartitivirus 1, a novel virus from Camellia oleifera

Brief Report

Absence of bovine leukemia virus proviral DNA in Japanese human blood cell lines and human cancer cell lines

Annotated Sequence Record

Genomic characterization of bacteriophage pEt-SU, a novel phiKZ-related virus infecting Edwardsiella tarda

Original Article

Proteomic and phosphoproteomic analyses reveal several events involved in the early stages of bovine herpesvirus 1 infection
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits