An outbreak of severe infections among Australian infants caused by a novel recombinant strain of human parechovirus type 3

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Nelson, Tiffanie M ^a,b   Vuillermin, Peter ^b,c   Hodge, Jason ^a,c   Druce, Julian ^a   Williams, David T ^d,e   Jasrotia, Rekha ^c   Alexandersen, Soren ^a,b,c  

^a University Hospital Geelong   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

^c BARWON HEALTH   (Australia)

^d PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^e CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; VIRUS RNA;

AUSTRALIA; DNA SEQUENCE; EPIDEMIC; GENETICS; GENOTYPE; HUMAN; INFANT; ISOLATION AND PURIFICATION; OPEN READING FRAME; PARECHOVIRUS; PATHOGENICITY; PATHOLOGY; PHYLOGENY; PICORNAVIRUS INFECTION; VIROLOGY; VIRUS GENOME;

AUSTRALIA; CAPSID PROTEINS; DISEASE OUTBREAKS; GENOME, VIRAL; GENOTYPE; HUMANS; INFANT; OPEN READING FRAMES; PARECHOVIRUS; PHYLOGENY; PICORNAVIRIDAE INFECTIONS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 85015199332     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44423     Document Type: Article

References (90)

1. Minor, P. The polio endgame. Hum Vaccin Immunother 10, 2106-2108, doi: 10.4161/21645515.2014.981115 (2014).
2. Alexandersen, S., Zhang, Z., Donaldson, A. I. & Garland, A. J. The pathogenesis and diagnosis of foot-And-mouth disease. J Comp Pathol 129, 1-36 (2003).
3. Harvala, H. & Simmonds, P. Human parechoviruses: biology, epidemiology and clinical significance. J Clin Virol 45, 1-9, doi: 10.1016/j.jcv.2009.03.009 (2009).
4. Mayo, M. A. & Pringle, C. R. Virus taxonomy-1997. J Gen Virol 79 (Pt 4), 649-657, doi: 10.1099/0022-1317-79-4-649 (1998).
5. Ghazi, F., Hughes, P. J., Hyypia, T. & Stanway, G. Molecular analysis of human parechovirus type 2 (formerly echovirus 23). J Gen Virol 79 (Pt 11), 2641-2650, doi: 10.1099/0022-1317-79-11-2641 (1998).
6. Coller, B. A. et al. Echovirus 22 is an atypical enterovirus. J Virol 64, 2692-2701 (1990).
7. Coller, B. G., Tracy, S. M. & Etchison, D. Cap-binding complex protein p220 is not cleaved during echovirus 22 replication in HeLa cells. J Virol 65, 3903-3905 (1991).
8. Al-Sunaidi, M., Williams, C. H., Hughes, P. J., Schnurr, D. P. & Stanway, G. Analysis of a new human parechovirus allows the definition of parechovirus types and the identification of RNA structural domains. J Virol 81, 1013-1021, doi: 10.1128/JVI.00584-06 (2007).
9. Nateri, A. S., Hughes, P. J. & Stanway, G. Terminal RNA replication elements in human parechovirus 1. J Virol 76, 13116-13122 (2002).
10. Nateri, A. S., Hughes, P. J. & Stanway, G. In vivo and in vitro identification of structural and sequence elements of the human parechovirus 5? untranslated region required for internal initiation. J Virol 74, 6269-6277 (2000).
11. Stanway, G. et al. Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. J Virol 68, 8232-8238 (1994).
12. Ito, M., Yamashita, T., Tsuzuki, H., Takeda, N. & Sakae, K. Isolation and identification of a novel human parechovirus. J Gen Virol 85, 391-398, doi: 10.1099/vir.0.19456-0 (2004).
13. Pulli, T., Koivunen, E. & Hyypia, T. Cell-surface interactions of echovirus 22. J Biol Chem 272, 21176-21180 (1997).
14. Alam, M. M. et al. Human parechovirus genotypes ? 10, ? 13 and ? 15 in Pakistani children with acute dehydrating gastroenteritis. PLoS One 8, e78377, doi: 10.1371/journal.pone.0078377 (2013).
15. Zhu, L. et al. Structure of Ljungan virus provides insight into genome packaging of this picornavirus. Nat Commun 6, 8316, doi: 10.1038/ncomms9316 (2015).
16. Jaaskelainen, A. J. et al. Serological survey in the Finnish human population implies human-To-human transmission of Ljungan virus or antigenically related viruses. Epidemiol Infect 144, 1278-1285, doi: 10.1017/S0950268815002551 (2016).
17. Nix, W. A. et al. Diversity of picornaviruses in rural Bolivia. J Gen Virol 94, 2017-2028, doi: 10.1099/vir.0.053827-0 (2013).
18. Bissel, S. J. et al. Human Parechovirus 3 Meningitis and Fatal Leukoencephalopathy. J Neuropathol Exp Neurol 74, 767-777, doi: 10.1097/NEN.0000000000000215 (2015).
19. Benschop, K. S. et al. Comprehensive full-length sequence analyses of human parechoviruses: diversity and recombination. J Gen Virol 91, 145-154, doi: 10.1099/vir.0.014670-0 (2010).
20. Zoll, J., Galama, J. M. & van Kuppeveld, F. J. Identification of potential recombination breakpoints in human parechoviruses. J Virol 83, 3379-3383, doi: 10.1128/JVI.02529-08 (2009).
21. Williams, C. H. et al. Evolution and conservation in human parechovirus genomes. J Gen Virol 90, 1702-1712, doi: 10.1099/vir.0.008813-0 (2009).
22. Zhu, R. et al. Characteristics of the mosaic genome of a human parechovirus type 1 strain isolated from an infant with pneumonia in China. Infect Genet Evol 29, 91-98, doi: 10.1016/j.meegid.2014.11.006 (2015).
23. Thoi, T. C., Than, V. T. & Kim, W. Whole genomic characterization of a Korean human parechovirus type 1 (HPeV1) identifies recombination events. J Med Virol 86, 2084-2091, doi: 10.1002/jmv.23921 (2014).
24. Calvert, J. et al. Recombination dynamics of human parechoviruses: investigation of type-specific differences in frequency and epidemiological correlates. J Gen Virol 91, 1229-1238, doi: 10.1099/vir.0.018747-0 (2010).
25. Benschop, K. S., Williams, C. H., Wolthers, K. C., Stanway, G. & Simmonds, P. Widespread recombination within human parechoviruses: Analysis of temporal dynamics and constraints. J Gen Virol 89, 1030-1035, doi: 10.1099/vir.0.83498-0 (2008).
26. Chieochansin, T., Vichiwattana, P., Korkong, S., Theamboonlers, A. & Poovorawan, Y. Molecular epidemiology, genome characterization, and recombination event of human parechovirus. Virology 421, 159-166, doi: 10.1016/j.virol.2011.09.021 (2011).
27. Drexler, J. F. et al. Full genome sequence analysis of parechoviruses from Brazil reveals geographical patterns in the evolution of non-structural genes and intratypic recombination in the capsid region. J Gen Virol 92, 564-571, doi: 10.1099/vir.0.022525-0 (2011).
28. Chen, H. F. et al. Diversity and recombination of human parechovirus in children with acute gastroenteritis in Guangzhou, China. J Med Virol 87, 296-302, doi: 10.1002/jmv.24030 (2015).
29. Benschop, K. S. et al. Fourth human parechovirus serotype. Emerg Infect Dis 12, 1572-1575, doi: 10.3201/eid1210.051647 (2006).
30. Fischer, T. K., Midgley, S., Dalgaard, C. & Nielsen, A. Y. Human parechovirus infection, Denmark. Emerg Infect Dis 20, 83-87, doi: 10.3201/eid2001.130569 (2014).
31. Harvala, H. et al. Comparison of diagnostic clinical samples and environmental sampling for enterovirus and parechovirus surveillance in Scotland, 2010 to 2012. Euro Surveill 19 (2014).
32. Boivin, G., Abed, Y. & Boucher, F. D. Human parechovirus 3 and neonatal infections. Emerg Infect Dis 11, 103-105, doi: 10.3201/eid1101.040606 (2005).
33. Harvala, H. et al. Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 199, 1753-1760, doi: 10.1086/599094 (2009).
34. Cordey, S. et al. Enterovirus and Parechovirus viraemia in young children presenting to the emergency room: Unrecognised and frequent. J Clin Virol 68, 69-72, doi: 10.1016/j.jcv.2015.05.003 (2015).
35. de Crom, S. C., Rossen, J. W., van Furth, A. M. & Obihara, C. C. Enterovirus and parechovirus infection in children: A brief overview. Eur J Pediatr 175, 1023-1029, doi: 10.1007/s00431-016-2725-7 (2016).
36. Cabrerizo, M. et al. Comparison of epidemiology and clinical characteristics of infections by human parechovirus vs.Those by enterovirus during the first month of life. Eur J Pediatr 174, 1511-1516, doi: 10.1007/s00431-015-2566-9 (2015).
37. Skram, M. K. et al. Severe parechovirus infection in Norwegian infants. Pediatr Infect Dis J 33, 1222-1225, doi: 10.1097/INF.0000000000000456 (2014).
38. Abed, Y. & Boivin, G. Molecular characterization of a Canadian human parechovirus (HPeV)-3 isolate and its relationship to other HPeVs. J Med Virol 77, 566-570, doi: 10.1002/jmv.20493 (2005).
39. Verboon-Maciolek, M. A. et al. Human parechovirus causes encephalitis with white matter injury in neonates. Ann Neurol 64, 266-273, doi: 10.1002/ana.21445 (2008).
40. Britton, P. N. et al. Parechovirus Encephalitis and Neurodevelopmental Outcomes. Pediatrics 137, e20152848, doi: 10.1542/peds.2015-2848 (2016).
41. Cooper, M. S., van Schilfgaarde, K. D., De Mel, G. R. & Rajapaksa, S. Identification of human parechovirus-3 in young infants within rural Victoria. J Paediatr Child Health 50, 746-747, doi: 10.1111/jpc.12704 (2014).
42. Cumming, G. et al. Parechovirus Genotype 3 Outbreak among Infants, New South Wales, Australia, 2013-2014. Emerg Infect Dis 21, 1144-1152, doi: 10.3201/eid2107.141149 (2015).
43. Khatami, A. et al. Sepsis-like disease in infants due to human parechovirus type 3 during an outbreak in Australia. Clin Infect Dis 60, 228-236, doi: 10.1093/cid/ciu784 (2015).
44. Aizawa, Y. et al. Role of Maternal Antibodies in Infants with Severe Diseases Related to Human Parechovirus Type 3. Emerg Infect Dis 21, 1966-1972, doi: 10.3201/eid2111.150267 (2015).
45. Aizawa, Y., Yamanaka, T., Watanabe, K., Oishi, T. & Saitoh, A. Asymptomatic children might transmit human parechovirus type 3 to neonates and young infants. J Clin Virol 70, 105-108, doi: 10.1016/j.jcv.2015.07.300 (2015).
46. Nielsen, N. M., Midgley, S. E., Nielsen, A. C., Christiansen, C. B. & Fischer, T. K. Severe Human Parechovirus Infections in Infants and the Role of Older Siblings. Am J Epidemiol 183, 664-670, doi: 10.1093/aje/kwv206 (2016).
47. Westerhuis, B. M., Jonker, S. C., Mattao, S., Benschop, K. S. & Wolthers, K. C. Growth characteristics of human parechovirus 1 to 6 on different cell lines and cross-neutralization of human parechovirus antibodies: A comparison of the cytopathic effect and real time PCR. Virol J 10, 146, doi: 10.1186/1743-422X-10-146 (2013).
48. Westerhuis, B. M. et al. Specific cell tropism and neutralization of human parechovirus types 1 and 3: implications for pathogenesis and therapy development. J Gen Virol 93, 2363-2370, doi: 10.1099/vir.0.043323-0 (2012).
49. Faria, N. R., de Vries, M., van Hemert, F. J., Benschop, K. & van der Hoek, L. Rooting human parechovirus evolution in time. BMC Evol Biol 9, 164, doi: 10.1186/1471-2148-9-164 (2009).
50. Mizuta, K. et al. Epidemic myalgia in adults associated with human parechovirus type 3 infection, Yamagata, Japan, 2008. Emerg Infect Dis 18, 1787-1793, doi: 10.3201/eid1811.111570 (2012).
51. Mizuta, K. et al. Epidemic myalgia and myositis associated with human parechovirus type 3 infections occur not only in adults but also in children: findings in Yamagata, Japan, 2014. Epidemiol Infect 144, 1286-1290, doi: 10.1017/S0950268815002873 (2016).
52. Mizuta, K. et al. Epidemic myalgia associated with human parechovirus type 3 infection among adults occurs during an outbreak among children: findings from Yamagata, Japan, in 2011. J Clin Virol 58, 188-193, doi: 10.1016/j.jcv.2013.05.019 (2013).
53. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948, doi: 10.1093/bioinformatics/btm404 (2007).
54. Lole, K. S. et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152-160 (1999).
55. Martin, D. P., Posada, D., Crandall, K. A. & Williamson, C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21, 98-102, doi: 10.1089/aid.2005.21.98 (2005).
56. Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D. GARD: A genetic algorithm for recombination detection. Bioinformatics 22, 3096-3098, doi: 10.1093/bioinformatics/btl474 (2006).
57. Delport, W., Poon, A. F. & Frost, S. D. & Kosakovsky Pond, S. L. Datamonkey 2010: A suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26, 2455-2457, doi: 10.1093/bioinformatics/btq429 (2010).
58. Kosakovsky Pond, S. L. et al. An evolutionary model-based algorithm for accurate phylogenetic breakpoint mapping and subtype prediction in HIV-1. PLoS Comput Biol 5, e1000581, doi: 10.1371/journal.pcbi.1000581 (2009).
59. Pond, S. L., Frost, S. D. & Muse, S. V. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676-679, doi: 10.1093/bioinformatics/bti079 (2005).
60. Pond, S. L. & Frost, S. D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531-2533, doi: 10.1093/bioinformatics/bti320 (2005).
61. Martin, D. & Rybicki, E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562-563 (2000).
62. Padidam, M., Sawyer, S. & Fauquet, C. M. Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218-225, doi: 10.1006/viro.1999.0056 (1999).
63. Smith, J. M. Analyzing the mosaic structure of genes. J Mol Evol 34, 126-129 (1992).
64. Posada, D. & Crandall, K. A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98, 13757-13762, doi: 10.1073/pnas.241370698 (2001).
65. Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. Sister-scanning: A Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573-582 (2000).
66. Boni, M. F., Posada, D. & Feldman, M. W. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176, 1035-1047, doi: 10.1534/genetics.106.068874 (2007).
67. Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution 1 (2015).
68. Joffret, M. L. et al. Genomic characterization of Sebokele virus 1 (SEBV1) reveals a new candidate species among the genus Parechovirus. J Gen Virol 94, 1547-1553, doi: 10.1099/vir.0.053157-0 (2013).
69. Smits, S. L. et al. Metagenomic analysis of the ferret fecal viral flora. PLoS One 8, e71595, doi: 10.1371/journal.pone.0071595 (2013).
70. Ekstrom, J. O., Tolf, C., Edman, K. A. & Lindberg, A. M. Physicochemical properties of the Ljungan virus prototype virion in different environments: inactivated by heat but resistant to acidic pH, detergents and non-physiological environments such as Virkon-containing solutions. Microbiol Immunol 51, 841-850 (2007).
71. Ekstrom, J. O. et al. Replication of Ljungan virus in cell culture: The genomic 5?-end, infectious cDNA clones and host cell response to viral infections. Virus Res 130, 129-139, doi: 10.1016/j.virusres.2007.06.004 (2007).
72. Jaaskelainen, A. J. et al. Evidence of Ljungan virus specific antibodies in humans and rodents, Finland. J Med Virol 85, 2001-2008, doi: 10.1002/jmv.23681 (2013).
73. Niklasson, B. Current views on Ljungan virus and its relationship to human diabetes. J Med Virol 83, 1673, doi: 10.1002/jmv.22062 (2011).
74. Niklasson, B., Samsioe, A., Papadogiannakis, N., Gustafsson, S. & Klitz, W. Zoonotic Ljungan virus associated with central nervous system malformations in terminated pregnancy. Birth Defects Res A Clin Mol Teratol 85, 542-545, doi: 10.1002/bdra.20568 (2009).
75. Niklasson, B. et al. Association of zoonotic Ljungan virus with intrauterine fetal deaths. Birth Defects Res A Clin Mol Teratol 79, 488-493, doi: 10.1002/bdra.20359 (2007).
76. Samsioe, A. et al. Ljungan virus present in intrauterine fetal death diagnosed by both immunohistochemistry and PCR. Birth Defects Res A Clin Mol Teratol 85, 227-229, doi: 10.1002/bdra.20554 (2009).
77. Sauvage, V. et al. A member of a new Picornaviridae genus is shed in pig feces. J Virol 86, 10036-10046, doi: 10.1128/JVI.00046-12 (2012).
78. Yu, J. M. et al. Identification of a novel picornavirus in healthy piglets and seroepidemiological evidence of its presence in humans. PLoS One 8, e70137, doi: 10.1371/journal.pone.0070137 (2013).
79. Reuter, G., Pankovics, P., Knowles, N. J. & Boros, A. Two closely related novel picornaviruses in cattle and sheep in Hungary from 2008 to 2009, proposed as members of a new genus in the family Picornaviridae. J Virol 86, 13295-13302, doi: 10.1128/JVI.01142-12 (2012).
80. Shan, T. L. et al. Human parechovirus infections in monkeys with diarrhea, China. Emerg Infect Dis 16, 1168-1169, doi: 10.3201/eid1607.091103 (2010).
81. Oberste, M. S. et al. Characterizing the picornavirus landscape among synanthropic nonhuman primates in Bangladesh, 2007 to 2008. J Virol 87, 558-571, doi: 10.1128/JVI.00837-12 (2013).
82. Bruhn, C. A. et al. Viral meningitis epidemics and a single, recent, recombinant and anthroponotic origin of swine vesicular disease virus. Evol Med Public Health 2015, 289-303, doi: 10.1093/emph/eov026 (2015).
83. Papadakis, G., Chibo, D., Druce, J., Catton, M. & Birch, C. Detection and genotyping of enteroviruses in cerebrospinal fluid in patients in Victoria, Australia, 2007-2013. J Med Virol 86, 1609-1613, doi: 10.1002/jmv.23885 (2014).
84. Nix, W. A., Maher, K., Pallansch, M. A. & Oberste, M. S. Parechovirus typing in clinical specimens by nested or semi-nested PCR coupled with sequencing. J Clin Virol 48, 202-207, doi: 10.1016/j.jcv.2010.04.007 (2010).
85. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30, 2725-2729, doi: 10.1093/molbev/mst197 (2013).
86. Bankevich, A. et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J Comput Biol 19, 455-477, doi: 10.1089/cmb.2012.0021 (2012).
87. Chevreux, B. et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14, 1147-1159, doi: 10.1101/gr.1917404 (2004).
88. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14, 178-192, doi: 10.1093/bib/bbs017 (2013).
89. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J Mol Biol 215, 403-410, doi: 10.1016/S0022-2836(05)80360-2 (1990).
90. Mount, D. W. Using the Basic Local Alignment Search Tool (BLAST). CSH Protoc 2007, pdb top17, doi: 10.1101/pdb.top17 (2007).