Predicting zoonotic risk of influenza a viruses from host tropism protein signature using random forest

International Journal of Molecular Sciences

Volumn 18, Issue 6, 2017, Pages

  Eng, Christine L P ^a   Tong, Joo Chuan ^b   Tan, Tin Wee ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b INSTITUTE OF HIGH PERFORMANCE COMPUTING   (Singapore)

^c Singapore National Supercomputing Centre (NSCC)   (Singapore)

Author keywords

Influenza; Machine learning; Zoonosis

Indexed keywords

AMINO ACID SEQUENCE; AREA UNDER THE CURVE; ARTICLE; AVIAN INFLUENZA; DIAGNOSTIC TEST ACCURACY STUDY; INFLUENZA A VIRUS; MACHINE LEARNING; NONHUMAN; PHYSICAL CHEMISTRY; PREDICTIVE VALUE; RANDOM FOREST; RECEIVER OPERATING CHARACTERISTIC; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; VIRAL TROPISM; ZOONOSIS; ANIMAL; BIRD; EPIDEMIC; GENETIC DATABASE; GENETICS; HOST PATHOGEN INTERACTION; HOST RANGE; HUMAN; INFLUENZA; ORTHOMYXOVIRUS INFECTION; REPRODUCIBILITY; THEORETICAL MODEL; VIROLOGY;

VIRAL PROTEIN;

ANIMALS; AREA UNDER CURVE; BIRDS; DATABASES, GENETIC; DISEASE OUTBREAKS; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MACHINE LEARNING; MODELS, THEORETICAL; ORTHOMYXOVIRIDAE INFECTIONS; REPRODUCIBILITY OF RESULTS; RETROSPECTIVE STUDIES; VIRAL PROTEINS; VIRAL TROPISM; ZOONOSES;

EID: 85019684178     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18061135     Document Type: Article

References (72)

1. Centers for Disease Control and Prevention. Isolation of avian influenza A (H5N1) viruses from humans-Hong Kong, May-December 1997. Morb. Mortal. Wkly. Rep. 1997, 46, 1204-1207.
2. Peiris, J.S.; de Jong, M.D.; Guan, Y. Avian influenza virus (H5N1): A threat to human health. Clin. Microbiol. Rev. 2007, 20, 243-267.
3. World Health Organization. Cumulative Number of Confirmed Human Cases for Avian Influenza A (H5N1) Reported to WHO, 2003-2016. Available online: http://www.who.int/influenza/human_animal_interface/EN_GIP_20160404cumulativenumberH5N1cases.pdf (accessed on 18 December 2016).
4. Fouchier, R.A.; Schneeberger, P.M.; Rozendaal, F.W.; Broekman, J.M.; Kemink, S.A.; Munster, V.; Kuiken, T.; Rimmelzwaan, G.F.; Schutten, M.; van Doornum, G.J. et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl. Acad. Sci. USA 2004, 101, 1356-1361.
5. Koopmans, M.; Wilbrink, B.; Conyn, M.; Natrop, G.; van der Nat, H.; Vennema, H.; Meijer, A.; van Steenbergen, J.; Fouchier, R.; Osterhaus, A. et al. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the netherlands. Lancet 2004, 363, 587-593.
6. Kurtz, J.; Manvell, R.J.; Banks, J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 1996, 348, 901-902.
7. Butt, K.M.; Smith, G.J.; Chen, H.; Zhang, L.J.; Leung, Y.H.; Xu, K.M.; Lim, W.; Webster, R.G.; Yuen, K.Y.; Peiris, J.S. et al. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J. Clin. Microbiol. 2005, 43, 5760-5767.
8. Peiris, M.; Yuen, K.Y.; Leung, C.W.; Chan, K.H.; Ip, P.L.; Lai, R.W.; Orr, W.K.; Shortridge, K.F. Human infection with influenza H9N2. Lancet 1999, 354, 916-917.
9. Chen, Y.; Liang, W.; Yang, S.; Wu, N.; Gao, H.; Sheng, J.; Yao, H.; Wo, J.; Fang, Q.; Cui, D.; et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: Clinical analysis and characterisation of viral genome. Lancet 2013, 381, 1916-1925.
10. Gao, R.; Cao, B.; Hu, Y.; Feng, Z.; Wang, D.; Hu, W.; Chen, J.; Jie, Z.; Qiu, H.; Xu, K. et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 2013, 368, 1888-1897.
11. Richard, M.; de Graaf, M.; Herfst, S. Avian influenza A viruses: From zoonosis to pandemic. Future Virol. 2014, 9, 513-524.
12. Yu, H.; Wu, J.T.; Cowling, B.J.; Liao, Q.; Fang, V.J.; Zhou, S.; Wu, P.; Zhou, H.; Lau, E.H.; Guo, D. et al. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: An ecological study. Lancet 2014, 383, 541-548.
13. World Health Organization. H5N1 Research Issues. Available online: http://www.who.int/influenza/human_animal_interface/avian_influenza/h5n1_research/en/ (accessed on 14 October 2014).
14. Heymann, D.L.; Dixon, M. Infections at the animal/human interface: Shifting the paradigm from emergency response to prevention at source. Curr. Top. Microbiol. Immunol. 2013, 366, 207-215.
15. Reid, A.H.; Taubenberger, J.K. The origin of the 1918 pandemic influenza virus: A continuing enigma. J. Gen. Virol. 2003, 84, 2285-2292.
16. Peiris, M.; Yen, H.L. Animal and human influenzas. Rev. Sci. Tech. 2014, 33, 539-553.
17. World Health Organization. Antigenic and Genetic Characteristics of Influenza A(H5N1) and Influenza A(H9N2) Viruses and Candidate Vaccine Viruses Developed for Potential Use in Human Vaccines. Available online: http://www.who.int/influenza/resources/documents/201009_H5_H9_VaccineVirusUpdate.pdf (accessed on 8 April 2014).
18. Chien, Y.J. How did international agencies perceive the avian influenza problem? The adoption and manufacture of the “one world, one health” framework. Soc. Health Illn. 2013, 35, 213-226.
19. Hartaningsih, N.; Wibawa, H.; Pudjiatmoko; Rasa, F.S.; Irianingsih, S.H.; Dharmawan, R.; Azhar, M.; Siregar, E.S.; McGrane, J.; Wong, F. et al. Surveillance at the molecular level: Developing an integrated network for detecting variation in avian influenza viruses in indonesia. Prev. Vet. Med. 2015, 120, 96-105.
20. Russell, C.A.; Kasson, P.M.; Donis, R.O.; Riley, S.; Dunbar, J.; Rambaut, A.; Asher, J.; Burke, S.; Davis, C.T.; Garten, R.J. et al. Improving pandemic influenza risk assessment. eLife 2014, 3, e03883.
21. Chen, G.W.; Chang, S.C.; Mok, C.K.; Lo, Y.L.; Kung, Y.N.; Huang, J.H.; Shih, Y.H.; Wang, J.Y.; Chiang, C.; Chen, C.J. et al. Genomic signatures of human versus avian influenza a viruses. Emerg. Infect. Dis. 2006, 12, 1353-1360.
22. Finkelstein, D.B.; Mukatira, S.; Mehta, P.K.; Obenauer, J.C.; Su, X.; Webster, R.G.; Naeve, C.W. Persistent host markers in pandemic and H5N1 influenza viruses. J. Virol. 2007, 81, 10292-10299.
23. Steel, J.; Lowen, A.C.; Mubareka, S.; Palese, P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 2009, 5, e1000252.
24. Subbarao, E.K.; London, W.; Murphy, B.R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol. 1993, 67, 1761-1764.
25. Khaliq, Z.; Leijon, M.; Belak, S.; Komorowski, J. Identification of combinatorial host-specific signatures with a potential to affect host adaptation in influenza A H1N1 and H3N2 subtypes. BMC Genom. 2016, 17, 529.
26. Sjaugi, M.F.; Tan, S.; Abd Raman, H.S.; Lim, W.C.; Nik Mohamed, N.E.; August, J.; Khan, A.M. g-FLUA2H: A web-based application to study the dynamics of animal-to-human mutation transmission for influenza viruses. BMC Med. Genom. 2015, 8, S5.
27. Taubenberger, J.K.; Kash, J.C. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 2010, 7, 440-451.
28. Global Influenza Programme. Tool for Influenza Pandemic Risk Assessment (TIPRA). Available online: http://www.who.int/influenza/publications/TIPRA_manual_v1/en/ (accessed on 14 March 2017).
29. Trock, S.C.; Burke, S.A.; Cox, N.J. Development of framework for assessing influenza virus pandemic risk. Emerg. Infect. Dis. 2015, 21, 1372-1378.
30. Qiang, X.; Kou, Z. Prediction of interspecies transmission for avian influenza A virus based on a back-propagation neural network. Math. Comput. Model. 2010, 52, 2060-2065.
31. Wang, J.; Ma, C.; Kou, Z.; Zhou, Y.; Liu, H. Predicting transmission of avian influenza A viruses from avian to human by using informative physicochemical properties. Int. J. Data Min. Bioinform. 2013, 7, 166-179.
32. Eng, C.L.; Tong, J.C.; Tan, T.W. Predicting host tropism of influenza A virus proteins using random forest. BMC Med. Genom. 2014, 7, S1.
33. Eng, C.L.; Tong, J.C.; Tan, T.W. Distinct host tropism protein signatures to identify possible zoonotic influenza A viruses. PLoS ONE 2016, 11, e0150173.
34. Kageyama, T.; Fujisaki, S.; Takashita, E.; Xu, H.; Yamada, S.; Uchida, Y.; Neumann, G.; Saito, T.; Kawaoka, Y.; Tashiro, M. Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 2013, 18, 20453.
35. World Health Organization. Overview of the Emergence and Characteristics of the Avian Influenza A(H7N9) Virus. Available online: Http://www.who.int/influenza/human_animal_interface/influenza_h7n9/WHO_H7N9_review_31May13.pdf?ua=1 (accessed on 8 April 2014).
36. Pantin-Jackwood, M.J.; Miller, P.J.; Spackman, E.; Swayne, D.E.; Susta, L.; Costa-Hurtado, M.; Suarez, D.L. Role of poultry in the spread of novel H7N9 influenza virus in china. J. Virol. 2014, 88, 5381-5390.
37. Yang, J.R.; Kuo, C.Y.; Huang, H.Y.; Wu, F.T.; Huang, Y.L.; Cheng, C.Y.; Su, Y.T.; Wu, H.S.; Liu, M.T. Characterization of influenza A (H7N9) viruses isolated from human cases imported into Taiwan. PLoS ONE 2015, 10, e0119792.
38. Rith, S.; Davis, C.T.; Duong, V.; Sar, B.; Horm, S.V.; Chin, S.; Ly, S.; Laurent, D.; Richner, B.; Oboho, I. et al. Identification of molecular markers associated with alteration of receptor-binding specificity in a novel genotype of highly pathogenic avian influenza A(H5N1) viruses detected in Cambodia in 2013. J. Virol. 2014, 88, 13897-13909.
39. Setiawaty, V.; Dharmayanti, N.L.; A Misriyah; Pawestri, H.A.; Azhar, M.; Tallis, G.; Schoonman, L.; Samaan, G. Avian influenza A(H5N1) virus outbreak investigation: Application of the FAO-OIE-WHO four-way linking framework in Indonesia. Zoonoses Public Health 2015, 62, 381-387.
40. Wibawa, H.; Henning, J.; Wong, F.; Selleck, P.; Junaidi, A.; Bingham, J.; Daniels, P.; Meers, J. A molecular and antigenic survey of H5N1 highly pathogenic avian influenza virus isolates from smallholder duck farms in Central Java, Indonesia during 2007-2008. J. Virol. 2011, 8, 425.
41. Breiman, L. Random forests. Mach. Learn. 2001, 45, 5-32.
42. Squires, R.B.; Noronha, J.; Hunt, V.; Garcia-Sastre, A.; Macken, C.; Baumgarth, N.; Suarez, D.; Pickett, B.E.; Zhang, Y.; Larsen, C.N. et al. Influenza research database: An integrated bioinformatics resource for influenza research and surveillance. Influenza Respir. Viruses 2012, 6, 404-416.
43. Ahmed, S.S.; Themudo, G.E.; Christensen, J.P.; Biswas, P.K.; Giasuddin, M.; Samad, M.A.; Toft, N.; Ersboll, A.K. Molecular epidemiology of circulating highly pathogenic avian influenza (H5N1) virus in chickens, in Bangladesh, 2007-2010. Vaccine 2012, 30, 7381-7390.
44. Centers for Disease Control and Prevention. Update: Influenza activity-United States and worldwide, 2005-06 season, and composition of the 2006-07 influenza vaccine. Morb. Mortal. Wkly. Rep. 2006, 55, 648-653.
45. Pabbaraju, K.; Tellier, R.; Wong, S.; Li, Y.; Bastien, N.; Tang, J.W.; Drews, S.J.; Jang, Y.; Davis, C.T.; Fonseca, K. et al. Full-genome analysis of avian influenza A(H5N1) virus from a human, North America, 2013. Emerg. Infect. Dis. 2014, 20, 887-891.
46. Rabinowitz, P.M.; Galusha, D.; Vegso, S.; Michalove, J.; Rinne, S.; Scotch, M.; Kane, M. Comparison of human and animal surveillance data for H5N1 influenza A in Egypt 2006-2011. PLoS ONE 2012, 7, e43851.
47. Claas, E.C.; de Jong, J.C.; van Beek, R.; Rimmelzwaan, G.F.; Osterhaus, A.D. Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine 1998, 16, 977-978.
48. Kandun, I.N.; Wibisono, H.; Sedyaningsih, E.R.; Yusharmen; Hadisoedarsuno, W.; Purba, W.; Santoso, H.; Septiawati, C.; Tresnaningsih, E.; Heriyanto, B. et al. Three Indonesian clusters of H5N1 virus infection in 2005. N. Engl. J. Med. 2006, 355, 2186-2194.
49. Centers for Disease Control and Prevention. Update: Influenza activity-United States and worldwide, 2006-07 season, and composition of the 2007-08 influenza vaccine. Morb. Mortal. Wkly. Rep. 2007, 56, 789-794.
50. Zaman, M.; Ashraf, S.; Dreyer, N.A.; Toovey, S. Human infection with avian influenza virus, Pakistan, 2007. Emerg. Infect. Dis. 2011, 17, 1056-1059.
51. Tiensin, T.; Chaitaweesub, P.; Songserm, T.; Chaisingh, A.; Hoonsuwan, W.; Buranathai, C.; Parakamawongsa, T.; Premashthira, S.; Amonsin, A.; Gilbert, M. et al. Highly pathogenic avian influenza H5N1, Thailand, 2004. Emerg. Infect. Dis. 2005, 11, 1664-1672.
52. Oner, A.F.; Bay, A.; Arslan, S.; Akdeniz, H.; Sahin, H.A.; Cesur, Y.; Epcacan, S.; Yilmaz, N.; Deger, I.; Kizilyildiz, B. et al. Avian influenza A (H5N1) infection in Eastern Turkey in 2006. N. Engl. J. Med. 2006, 355, 2179-2185.
53. Manabe, T.; Yamaoka, K.; Tango, T.; Binh, N.G.; Co, D.X.; Tuan, N.D.; Izumi, S.; Takasaki, J.; Chau, N.Q.; Kudo, K. Chronological, geographical, and seasonal trends of human cases of avian influenza A (H5N1) in Vietnam, 2003-2014: A spatial analysis. BMC Infect. Dis. 2016, 16, 64.
54. Qi, X.; Cui, L.; Yu, H.; Ge, Y.; Tang, F. Whole-genome sequence of a reassortant H5N6 avian influenza virus isolated from a live poultry market in China, 2013. Genome Announc. 2014, 2.
55. Yuan, J.; Zhang, L.; Kan, X.; Jiang, L.; Yang, J.; Guo, Z.; Ren, Q. Origin and molecular characteristics of a novel 2013 avian influenza A(H6N1) virus causing human infection in Taiwan. Clin. Infect. Dis. 2013, 57, 1367-1368.
56. Editorial Team. Avian influenza A/(H7N2) outbreak in the United Kingdom. Euro Surveill. 2007, 12, E070531.
57. Editorial team. Avian influenza H5N1 detected in poultry in Nigeria, further human cases reported in Iraq, Indonesia and China. Euro Surveill. 2006, 11, E060209 060201.
58. Ostrowsky, B.; Huang, A.; Terry, W.; Anton, D.; Brunagel, B.; Traynor, L.; Abid, S.; Johnson, G.; Kacica, M.; Katz, J. et al. Low pathogenic avian influenza A (H7N2) virus infection in immunocompromised adult, New York, USA, 2003. Emerg. Infect. Dis. 2012, 18, 1128-1131.
59. Tweed, S.A.; Skowronski, D.M.; Davies, T.M.; Larder, A.; Petric, M.; Lees, W.; Li, Y.; Katz, J.; Krajden, M.; Tellier, R. et al. Human illness from avian influenza H7N3, British Columbia. Emerg. Infect. Dis. 2004, 10, 2196-2199.
60. Puzelli, S.; di Trani, L.; Fabiani, C.; Campitelli, L.; de Marco, M.A.; Capua, I.; Aguilera, J.F.; Zambon, M.; Donatelli, I. Serological analysis of serum samples from humans exposed to avian H7 influenza viruses in Italy between 1999 and 2003. J. Infect. Dis. 2005, 192, 1318-1322.
61. Lopez-Martinez, I.; Balish, A.; Barrera-Badillo, G.; Jones, J.; Nunez-Garcia, T.E.; Jang, Y.; Aparicio-Antonio, R.; Azziz-Baumgartner, E.; Belser, J.A.; Ramirez-Gonzalez, J.E. et al. Highly pathogenic avian influenza A(H7N3) virus in poultry workers, Mexico, 2012. Emerg. Infect. Dis. 2013, 19, 1531-1534.
62. Nguyen-Van-Tam, J.S.; Nair, P.; Acheson, P.; Baker, A.; Barker, M.; Bracebridge, S.; Croft, J.; Ellis, J.; Gelletlie, R.; Gent, N.; et al. Outbreak of low pathogenicity H7N3 avian influenza in UK, including associated case of human conjunctivitis. Euro Surveill. 2006, 11, E060504 060502.
63. Puzelli, S.; Rossini, G.; Facchini, M.; Vaccari, G.; di Trani, L.; di Martino, A.; Gaibani, P.; Vocale, C.; Cattoli, G.; Bennett, M. et al. Human infection with highly pathogenic A(H7N7) avian influenza virus, Italy, 2013. Emerg. Infect. Dis. 2014, 20, 1745-1749.
64. World Health Organization. Background and Summary of Human Infection with Avian Influenza A(H7N9) Virus-As of 31 January 2014. Available online: http://www.who.int/influenza/human_animal_interface/20140131_background_and_summary_H7N9_v1.pdf?ua=1 (accessed on 21 December 2016).
65. Huang, Y.; Li, X.; Zhang, H.; Chen, B.; Jiang, Y.; Yang, L.; Zhu, W.; Hu, S.; Zhou, S.; Tang, Y. et al. Human infection with an avian influenza A (H9N2) virus in the middle region of China. J. Med. Virol. 2015, 87, 1641-1648.
66. Pan American Health Organization. Avian Influenza Virus A(H10N7) Circulating among Humans in Egypt. Available online: http://www1.paho.org/hq/dmdocuments/2010/Avian_Influenza_Egypt_070503.pdf (accessed on 17 December 2016).
67. Arzey, G.G.; Kirkland, P.D.; Arzey, K.E.; Frost, M.; Maywood, P.; Conaty, S.; Hurt, A.C.; Deng, Y.M.; Iannello, P.; Barr, I. et al. Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia. Emerg. Infect. Dis. 2012, 18, 814-816.
68. Chen, H.; Yuan, H.; Gao, R.; Zhang, J.; Wang, D.; Xiong, Y.; Fan, G.; Yang, F.; Li, X.; Zhou, J. et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: A descriptive study. Lancet 2014, 383, 714-721.
69. Hall, M.; Frank, E.; Holmes, G.; Pfahringer, B.; Reutemann, P.; Witten, I.H. The WEKA data mining software: An update. SIGKDD Explor. 2009, 11, 10-18.
70. Fawcett, T. An introduction to ROC analysis. Pattern Recogn. Lett. 2006, 27, 861-874.
71. Linden, A. Measuring diagnostic and predictive accuracy in disease management: An introduction to receiver operating characteristic (ROC) analysis. J. Eval. Clin. Pract. 2006, 12, 132-139.
72. Herrick, K.A.; Huettmann, F.; Lindgren, M.A. A global model of avian influenza prediction in wild birds: The importance of northern regions. BMC Vet. Res. 2013, 44, 42.