1932

Abstract

Parvoviruses are structurally simple viruses with linear single-stranded DNA genomes and nonenveloped icosahedral capsids. They infect a wide range of animals from insects to humans. Parvovirus B19 is a long-known human pathogen, whereas adeno-associated viruses are nonpathogenic. Since 2005, many parvoviruses have been discovered in human-derived samples: bocaviruses 1–4, parvovirus 4, bufavirus, tusavirus, and cutavirus. Some human parvoviruses have already been shown to cause disease during acute infection, some are associated with chronic diseases, and others still remain to be proven clinically relevant—or harmless commensals, a distinction not as apparent as it might seem. One initially human-labeled parvovirus might not even be a human virus, whereas another was originally overlooked due to inadequate diagnostics. The intention of this review is to follow the rocky road of emerging human parvoviruses from discovery of a DNA sequence to current and future clinical status, highlighting the perils along the way.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-092818-015803
2019-09-29
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/virology/6/1/annurev-virology-092818-015803.html?itemId=/content/journals/10.1146/annurev-virology-092818-015803&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Qiu J, Söderlund-Venermo M, Young NS 2017. Human parvoviruses. Clin. Microbiol. Rev. 30:43–113
    [Google Scholar]
  2. 2. 
    Matthews PC, Sharp C, Simmonds P, Klenerman P 2017. Human parvovirus 4 ‘PARV4’ remains elusive despite a decade of study. F1000Research 6:82
    [Google Scholar]
  3. 3. 
    Väisänen E, Fu Y, Hedman K, Söderlund-Venermo M 2017. Human protoparvoviruses. Viruses 9:354
    [Google Scholar]
  4. 4. 
    Ong DSY, Schuurman R, Heikens E 2016. Human bocavirus in stool: a true pathogen or an innocent bystander?. J. Clin. Virol. 74:45–49
    [Google Scholar]
  5. 5. 
    Jartti T, Hedman K, Jartti L, Ruuskanen O, Allander T, Söderlund-Venermo M 2012. Human bocavirus—the first 5 years. Rev. Med. Virol. 22:46–64
    [Google Scholar]
  6. 6. 
    Christensen A, Kesti O, Elenius V, Eskola A, Døllner H et al. 2019. Human bocaviruses and paediatric infections. Lancet Child Adolesc. Health 3:418–26
    [Google Scholar]
  7. 7. 
    Atchison RW, Castro BC, Hammon W 1965. Adenovirus-associated defective virus particles. Science 149:754–55
    [Google Scholar]
  8. 8. 
    Cossart YE, Field AM, Cant B, Widdows D 1975. Parvovirus-like particles in human sera. Lancet 1:72–73
    [Google Scholar]
  9. 9. 
    Nguyen QT, Sifer C, Schneider V, Bernaudin F, Auguste V, Garbarg-Chenon A 1998. Detection of an erythrovirus sequence distinct from B19 in a child with acute anaemia. Lancet 352:1524
    [Google Scholar]
  10. 10. 
    Hokynar K, Söderlund-Venermo M, Pesonen M, Ranki A, Partio EK, Hedman K 2002. A new parvovirus genotype persistent in human skin. Virology 302:224–28
    [Google Scholar]
  11. 11. 
    Servant A, Laperche S, Lallemand F, Marinho V, De Saint Maur G et al. 2002. Genetic diversity within human erythroviruses: identification of three genotypes. J. Virol. 76:9124–34
    [Google Scholar]
  12. 12. 
    Nguyen QT, Wong S, Heegard ED, Brown KE 2002. Identification and characterization of a second novel human Erythrovirus variant, A6. Virology 301:374–80
    [Google Scholar]
  13. 13. 
    Jones MS, Kapoor A, Lukashov VV, Simmonds P, Hecht F, Delwart E 2005. New DNA viruses identified in patients with acute viral infection syndrome. J. Virol. 79:8230–36
    [Google Scholar]
  14. 14. 
    Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B 2005. Cloning of a human parvovirus by molecular screening of respiratory tract samples. PNAS 102:12891–96
    [Google Scholar]
  15. 15. 
    Arthur JL, Higgins GD, Davidson GP, Givney RC, Ratcliff RM 2009. A novel bocavirus associated with acute gastroenteritis in Australian children. PLOS Pathog 5:e1000391
    [Google Scholar]
  16. 16. 
    Kapoor A, Slikas E, Simmonds P, Chieochansin T, Naeem A et al. 2009. A newly identified bocavirus species in human stool. J. Infect. Dis. 199:196–200
    [Google Scholar]
  17. 17. 
    Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L et al. 2010. Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J. Infect. Dis. 201:1633–43
    [Google Scholar]
  18. 18. 
    Phan TG, Vo NP, Bonkoungou IJ, Kapoor A, Barro N et al. 2012. Acute diarrhea in West African children: diverse enteric viruses and a novel parvovirus genus. J. Virol. 86:11024–30
    [Google Scholar]
  19. 19. 
    Phan TG, Sdiri-Loulizi K, Aouni M, Ambert-Balay K, Pothier P et al. 2014. New parvovirus in child with unexplained diarrhea, Tunisia. Emerg. Infect. Dis. 20:1911–13
    [Google Scholar]
  20. 20. 
    Phan TG, Dreno B, da Costa AC, Li L, Orlandi P et al. 2016. A new protoparvovirus in human fecal samples and cutaneous T cell lymphomas (mycosis fungoides). Virology 496:299–305
    [Google Scholar]
  21. 21. 
    Paver WK, Caul EO, Ashley CR, Clarke SKR 1973. A small virus in human faeces. Lancet 1:237–40
    [Google Scholar]
  22. 22. 
    Naccache SN, Greninger AL, Lee D, Coffey LL, Phan T et al. 2013. The perils of pathogen discovery: origin of a novel parvovirus-like hybrid genome traced to nucleic acid extraction spin columns. J. Virol. 87:11966–77
    [Google Scholar]
  23. 23. 
    Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hübinger AM et al. 2019. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol. 100:367–68
    [Google Scholar]
  24. 24. 
    Kilham L, Olivier LJ. 1959. A latent virus of rats isolated in tissue culture. Virology 7:428–37
    [Google Scholar]
  25. 25. 
    Huang Q, Deng X, Yan Z, Cheng F, Luo Y et al. 2012. Establishment of a reverse genetics system for studying human bocavirus in human airway epithelia. PLOS Pathog 8:e1002899
    [Google Scholar]
  26. 26. 
    Zou W, Cheng F, Shen W, Engelhardt JF, Yan Z, Qiu J 2016. Nonstructural protein NP1 of human bocavirus 1 plays a critical role in the expression of viral capsid proteins. J. Virol. 90:4658–69
    [Google Scholar]
  27. 27. 
    Wang Z, Shen W, Cheng F, Deng X, Engelhardt JF et al. 2017. Parvovirus expresses a small noncoding RNA that plays an essential role in virus replication. J. Virol. 91:e02375–16
    [Google Scholar]
  28. 28. 
    Kajigaya S, Fujii H, Field A, Anderson S, Rosenfeld S et al. 1991. Self-assembled B19 parvovirus capsids, produced in a baculovirus system, are antigenically and immunogenically similar to native virions. PNAS 88:4646–50
    [Google Scholar]
  29. 29. 
    Brown CS, van Lent JWM, Vlak JM, Spaan WJM 1991. Assembly of empty capsids by using baculovirus recombinants expressing human parvovirus B19 structural protein. J. Virol. 65:2702–6
    [Google Scholar]
  30. 30. 
    Lin F, Guan W, Cheng F, Yang N, Pintel D, Qiu J 2008. ELISAs using human bocavirus VP2 virus-like particles for detection of antibodies against HBoV. J. Virol. Methods 149:110–17
    [Google Scholar]
  31. 31. 
    Kahn JS, Kesebir D, Cotmore SF, D'Abramo A Jr., Cosby C et al. 2008. Seroepidemiology of human bocavirus defined using recombinant virus-like particles. J. Infect. Dis. 198:41–50
    [Google Scholar]
  32. 32. 
    Lindner J, Karalar L, Zehentmeier S, Plentz A, Pfister H et al. 2008. Humoral immune response against human bocavirus VP2 virus-like particles. Viral Immunol 21:443–49
    [Google Scholar]
  33. 33. 
    Söderlund-Venermo M, Lahtinen A, Jartti T, Hedman L, Kemppainen K et al. 2009. Clinical assessment and improved diagnosis of bocavirus-induced wheezing in children, Finland. Emerg. Infect. Dis. 15:1423–29
    [Google Scholar]
  34. 34. 
    Sharp CP, Lail A, Donfield S, Simmons R, Leen C et al. 2009. High frequencies of exposure to the novel human parvovirus PARV4 in hemophiliacs and injection drug users, as detected by a serological assay for PARV4 antibodies. J. Infect. Dis. 200:1119–25
    [Google Scholar]
  35. 35. 
    Lahtinen A, Kivelä P, Hedman L, Kumar A, Kantele A et al. 2011. Serodiagnosis of primary infections with human parvovirus 4, Finland. Emerg. Infect. Dis. 17:79–82
    [Google Scholar]
  36. 36. 
    Tamosiunas PL, Petraityte-Burneikiene R, Bulavaite A, Marcinkeviciute K, Simutis K et al. 2016. Yeast-generated virus-like particles as antigens for detection of human bocavirus 1–4 specific antibodies in human serum. Appl. Microbiol. Biotechnol. 100:4935–46
    [Google Scholar]
  37. 37. 
    Väisänen E, Paloniemi M, Kuisma I, Lithovius V, Kumar A et al. 2016. Epidemiology of two human protoparvoviruses, bufavirus and tusavirus. Sci. Rep. 6:39267
    [Google Scholar]
  38. 38. 
    Väisänen E, Mohanraj U, Kinnunen P, Jokelainen P, Al-Hello H et al. 2018. Global distribution of human protoparvoviruses. Emerg. Infect. Dis. 24:1292–99
    [Google Scholar]
  39. 39. 
    Halder S, Ng R, Agbandje-McKenna M 2012. Parvoviruses: structure and infection. Future Virol 7:253–78
    [Google Scholar]
  40. 40. 
    Kaufmann B, Simpson AA, Rossmann MG 2004. The structure of human parvovirus B19. PNAS 101:11628–33
    [Google Scholar]
  41. 41. 
    Gurda BL, Parent KN, Bladek H, Sinkovits RS, DiMattia MA et al. 2010. Human bocavirus capsid structure: insights into the structural repertoire of the Parvoviridae. J. Virol 84:5880–89
    [Google Scholar]
  42. 42. 
    Mietzsch M, Kailasan S, Garrison J, Ilyas M, Chipman P et al. 2017. Structural insights into human bocaparvoviruses. J. Virol. 91:e00261–17
    [Google Scholar]
  43. 43. 
    Ilyas M, Mietzsch M, Kailasan S, Väisänen E, Luo M et al. 2018. Atomic resolution structures of human bufaviruses determined by cryo-electron microscopy. Viruses 10:22
    [Google Scholar]
  44. 44. 
    Mietzsch M, Pénzes JJ, Agbandje-McKenna M 2019. Twenty-five years of structural parvovirology. Viruses 11:362
    [Google Scholar]
  45. 45. 
    Söderlund M, Brown KE, Meurman O, Hedman K 1992. Prokaryotic expression of a VP1 polypeptide antigen for diagnosis by a human parvovirus B19 antibody enzyme immunoassay. J. Clin. Microbiol. 30:305–11
    [Google Scholar]
  46. 46. 
    Saikawa T, Anderson S, Momoeda M, Kajigaya S, Young NS 1993. Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J. Virol. 67:3004–9
    [Google Scholar]
  47. 47. 
    Kantola K, Hedman L, Allander T, Jartti T, Lehtinen P et al. 2008. Serodiagnosis of human bocavirus infections. Clin. Infect. Dis. 46:540–46
    [Google Scholar]
  48. 48. 
    Leisi R, Ruprecht N, Kempf C, Ros C 2013. Parvovirus B19 uptake is a highly selective process controlled by VP1u, a novel determinant of viral tropism. J. Virol. 87:13161–67
    [Google Scholar]
  49. 49. 
    Kailasan S, Garrison J, Ilyas M, Chipman P, McKenna R et al. 2016. Mapping antigenic epitopes on the human bocavirus capsid. J. Virol. 90:4670–80
    [Google Scholar]
  50. 50. 
    Vihinen-Ranta M, Suikkanen S, Parrish CR 2004. Pathways of cell infection by parvoviruses and adeno-associated viruses. J. Virol. 78:6709–14
    [Google Scholar]
  51. 51. 
    Tattersall P, Ward DC. 1976. Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263:106–9
    [Google Scholar]
  52. 52. 
    Deng X, Yan Z, Cheng F, Engelhardt JF, Qiu J 2016. Replication of an autonomous human parvovirus in non-dividing human airway epithelium is facilitated through the DNA damage and repair pathways. PLOS Pathog 212:e1005399
    [Google Scholar]
  53. 53. 
    Fryer JF, Kapoor A, Minor PD, Delwart E, Baylis SA 2006. Novel parvovirus and related variant in human plasma. Emerg. Infect. Dis. 12:151–54
    [Google Scholar]
  54. 54. 
    Simmonds P, Manning A, Kenneil R, Carnie FW, Bell JE 2007. Parenteral transmission of the novel human parvovirus PARV4. Emerg. Infect. Dis. 13:1386–88
    [Google Scholar]
  55. 55. 
    Manning A, Willey SJ, Bell JE, Simmonds P 2007. Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J. Infect. Dis. 195:1345–52
    [Google Scholar]
  56. 56. 
    Longhi E, Bestetti G, Acquaviva V, Foschi A, Piolini R et al. 2007. Human parvovirus 4 in the bone marrow of Italian patients with AIDS. AIDS 21:1481–83
    [Google Scholar]
  57. 57. 
    Panning M, Kobble R, Vollbach, Drexler JF, Adjei S et al. 2010. Novel human parvovirus 4 genotype 3 in infants, Ghana. Emerg. Infect. Dis. 16:1143–46
    [Google Scholar]
  58. 58. 
    Drexler JF, Reber U, Muth D, Herzog P, Annan A et al. 2012. Human parvovirus 4 in nasal and fecal specimens from children, Ghana. Emerg. Infect. Dis. 18:1650–53
    [Google Scholar]
  59. 59. 
    von Linstow M-L, Høgh M, Høgh B 2008. Clinical and epidemiologic characteristics of human bocavirus in Danish infants. Pediatr. Infect. Dis. J. 27:897–902
    [Google Scholar]
  60. 60. 
    Longtin J, Bastien M, Gilca R, Leblanc E, de Serres G et al. 2008. Human bocavirus infections in hospitalized children and adults. Emerg. Infect. Dis. 14:217–21
    [Google Scholar]
  61. 61. 
    Martin ET, Kuypers J, McRoberts JP, Englund JA, Zerr DM 2015. Human bocavirus 1 primary infection and shedding in infants. J. Infect. Dis. 212:516–24
    [Google Scholar]
  62. 62. 
    Chieochansin T, Kapoor A, Delwart E, Poovorawan Y, Simmonds P 2009. Absence of detectable replication of human bocavirus species 2 in respiratory tract. Emerg. Infect. Dis. 15:1503–5
    [Google Scholar]
  63. 63. 
    Santos N, Peret TCT, Humphrey CD, Albuquerque MC, Silva RC et al. 2010. Human bocavirus species 2 and 3 in Brazil. J. Clin. Virol. 48:127–30
    [Google Scholar]
  64. 64. 
    Paloniemi M, Lappalainen S, Salminen M, Kätkä M, Kantola K et al. 2014. Human bocaviruses are commonly found in stools of hospitalized children without causal association to acute gastroenteritis. Eur. J. Pediatr. 173:1051–57
    [Google Scholar]
  65. 65. 
    Hamza IA, Jurzik L, Wilhelm M, Überla K 2009. Detection and quantification of human bocavirus in river water. J. Gen. Virol. 90:2634–37
    [Google Scholar]
  66. 66. 
    Blinkowa O, Rosario K, Li L, Kapoor A, Silikas B et al. 2009. Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States. J. Clin. Microbiol. 47:3507–13
    [Google Scholar]
  67. 67. 
    Myrmel M, Lange H, Rimstad E 2015. A 1-year quantitative survey of noro-, adeno-, human boca-, and hepatitis E viruses in raw and secondarily treated sewage from two plants in Norway. Food Environ. Virol. 7:213–23
    [Google Scholar]
  68. 68. 
    Guerrero-Latorre L, Romero B, Bonifaz E, Timoneda N, Rusinol M et al. 2018. Quito's virome: metagenomic analysis of viral diversity in urban streams of Ecuador's capital city. Sci. Total Environ. 645:1334–43
    [Google Scholar]
  69. 69. 
    Väisänen E, Kuisma I, Phan TG, Delwart E, Lappalainen M et al. 2014. Bufavirus in feces of patients with gastroenteritis, Finland. Emerg. Infect. Dis. 20:1077–80
    [Google Scholar]
  70. 70. 
    Yahiro T, Wangchuk S, Tshering K, Bandhari P, Zangmo S et al. 2014. Novel genotype 3 human bufavirus from children with severe diarrhea, Bhutan. Emerg. Infect. Dis. 20:1037–39
    [Google Scholar]
  71. 71. 
    Smits L, Schapendonk CM, van Beek J, Vennema H, Schurch AC et al. 2014. New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg. Infect. Dis. 20:1218–22
    [Google Scholar]
  72. 72. 
    Altay A, Yahiro T, Bozdayi G, Matsumoto T, Sahin F et al. 2015. Bufavirus genotype 3 in Turkish children with severe diarrhoea. Clin. Microbiol. Infect. 21:965.e1–4
    [Google Scholar]
  73. 73. 
    Chieochansin T, Vutithanachot V, Theamboonlers A, Poovorawan Y 2015. Bufavirus in fecal specimens of patients with and without diarrhea in Thailand. Arch. Virol. 160:1781–84
    [Google Scholar]
  74. 74. 
    Huang DD, Wang W, Lu QB, Zhao J, Guo CT et al. 2015. Identification of bufavirus-1 and bufavirus-3 in feces of patients with acute diarrhea, China. Sci. Rep. 5:13272
    [Google Scholar]
  75. 75. 
    Fridell E, Cohen B, Wahren B 1991. Evaluation of a synthetic-peptide enzyme-linked immuno-sorbent assay for immunoglobulin M to human parvovirus B19. J. Clin. Microbiol. 29:1376–81
    [Google Scholar]
  76. 76. 
    Endo R, Ishiguro N, Kikuta H, Teramoto S, Shirkoohi R et al. 2007. Seroepidemiology of human bocavirus in Hokkaido prefecture, Japan. J. Clin. Microbiol. 45:3218–23
    [Google Scholar]
  77. 77. 
    Söderlund M, Brown CS, Cohen BJ, Hedman K 1995. Accurate serodiagnosis of B19 parvovirus infections by measurement of IgG avidity. J. Infect. Dis. 171:710–13
    [Google Scholar]
  78. 78. 
    Söderlund M, Brown CS, Spaan WJM, Hedman L, Hedman K 1995. Epitope type-specific IgG responses to capsid proteins VP1 and VP2 of human parvovirus B19. J. Infect. Dis. 172:1431–36
    [Google Scholar]
  79. 79. 
    Kantola K, Hedman L, Arthur J, Alibet A, Delwart E et al. 2011. Seroepidemiology of human bocaviruses 1–4. J. Infect. Dis. 204:1403–12
    [Google Scholar]
  80. 80. 
    Väisänen E, Fu Y, Koskenmies S, Fyhrquist N, Wang Y et al. 2018. Cutavirus DNA in malignant and non-malignant skin of cutaneous T-cell lymphoma and organ transplant patients but not of healthy adults. Clin. Infect. Dis. 68:1904–10
    [Google Scholar]
  81. 81. 
    Ekman A, Hokynar K, Kakkola L, Kantola K, Bondén H et al. 2007. Biological and immunological relations of human parvovirus B19 genotypes 1–3. J. Virol. 81:6927–35
    [Google Scholar]
  82. 82. 
    Mossong J, Hens N, Friederichs V, Davidkin I, Broman M et al. 2008. Parvovirus B19 infection in five European countries: seroepidemiology, force of infection and maternal risk of infection. Epidemiol. Infect. 136:1059–68
    [Google Scholar]
  83. 83. 
    Guo L, Wang Y, Zhou H, Wu C, Song J et al. 2012. Differential seroprevalence of human bocavirus species 1–4 in Beijing, China. PLOS ONE 7:e39644
    [Google Scholar]
  84. 84. 
    Kantola K, Hedman L, Tanner L, Simell V, Mäkinen M et al. 2015. B-cell responses to human bocaviruses 1–4: new insights from childhood follow-up study. PLOS ONE 10:e0139096
    [Google Scholar]
  85. 85. 
    Li X, Kantola K, Hedman L, Arku B, Hedman K, Söderlund-Venermo M 2015. Original antigenic sin with human bocaviruses 1–4. J. Gen. Virol. 96:3099–108
    [Google Scholar]
  86. 86. 
    Francis T Jr 1960. On the doctrine of original antigenic sin. Proc. Am. Philos. Soc. 104:572–78
    [Google Scholar]
  87. 87. 
    Sharp CP, Gregory WF, Hattingh L, Malik A, Adland E et al. 2017. PARV4 prevalence, phylogeny, immunology and coinfection with HIV, HBV and HCV in a multicenter African cohort. Wellcome Open Res 2:26
    [Google Scholar]
  88. 88. 
    Chen T, Hedman L, Mattila PS, Jartti L, Jartti T et al. 2012. Biotin IgM antibodies in human blood: a previously unknown factor eliciting false results in biotinylation-based immunoassays. PLOS ONE 7:e42376
    [Google Scholar]
  89. 89. 
    Hedman K, Lappalainen M, Söderlund M, Hedman L 1993. Avidity of IgG in serodiagnosis of infectious diseases. Rev. Med. Microbiol. 4:123–29
    [Google Scholar]
  90. 90. 
    Kaikkonen L, Lankinen H, Harjunpää I, Hokynar K, Söderlund-Venermo M et al. 1999. Acute-phase-specific heptapeptide epitope for diagnosis of parvovirus B19 infection. J. Clin. Microbiol. 37:3952–56
    [Google Scholar]
  91. 91. 
    Gray JJ, Cohen BJ, Desselberger U 1993. Detection of human parvovirus Bl9-specific IgM and IgG antibodies using a recombinant viral VP1 antigen expressed in insect cells and estimation of time of infection by testing for antibody avidity. J. Virol. Methods 44:11–24
    [Google Scholar]
  92. 92. 
    Enders M, Weidner A, Rosenthal T, Baisch C, Hedman L et al. 2008. Improved diagnosis of gestational B19 parvovirus infection at the time of fetal hydrops. J. Infect. Dis. 197:58–62
    [Google Scholar]
  93. 93. 
    Hedman L, Söderlund-Venermo M, Jartti T, Ruuskanen O, Hedman K 2010. Dating of human bocavirus infection with protein-denaturing IgG-avidity assays—secondary immune activations are ubiquitous in immunocompetent adults. J. Clin. Virol. 48:44–48
    [Google Scholar]
  94. 94. 
    Maple PAC, Hedman L, Dhanilla P, Kantola K, Nurmi V et al. 2014. Identification of past and recent parvovirus B19V infection in immunocompetent individuals by quantitative PCR and enzyme immunoassays: a dual-laboratory study. J. Clin. Microbiol. 52:947–56
    [Google Scholar]
  95. 95. 
    Christensen A, Nordbo SA, Krokstad S, Rognlien AG, Dollner H 2010. Human bocavirus in children: Mono-detection, high viral load and viraemia are associated with respiratory tract infection. J. Clin. Virol. 49:158–62
    [Google Scholar]
  96. 96. 
    Zhao B, Yu X, Wang C, Teng Z, Wang C et al. 2013. High human bocavirus viral load is associated with disease severity in children under five years of age. PLOS ONE 8:e62318
    [Google Scholar]
  97. 97. 
    Fry AM, Lu X, Chittaganpitch M, Peret T, Fischer J et al. 2007. Human bocavirus: a novel parvovirus epidemiologically associated with pneumonia requiring hospitalization in Thailand. J. Infect. Dis. 195:1038–45
    [Google Scholar]
  98. 98. 
    Xu M, Arku B, Jartti T, Koskinen JO, Peltola V et al. 2017. Comparative diagnosis of human bocavirus 1 respiratory infection with messenger RNA reverse-transcription PCR, DNA quantitative PCR, and serology. J. Infect. Dis. 215:1551–57
    [Google Scholar]
  99. 99. 
    Proenca-Modena JL, Gagliardi TB, de Paula FE, Iwamoto MA, Criado MF et al. 2011. Detection of human bocavirus mRNA in respiratory secretions correlates with high viral load and concurrent diarrhea. PLOS ONE 6:e21083
    [Google Scholar]
  100. 100. 
    Christensen A, Dollner H, Skanke LH, Krokstad S, Moe N, Nordbo SA 2013. Detection of spliced mRNA from human bocavirus 1 in clinical samples from children with respiratory tract infections. Emerg. Infect. Dis. 19:574–80
    [Google Scholar]
  101. 101. 
    Schlaberg R, Ampofo K, Tardif KD, Stockmann C, Simmon KE et al. 2017. Human bocavirus capsid messenger RNA detection in children with pneumonia. J. Infect. Dis. 216:688–96
    [Google Scholar]
  102. 102. 
    Bruning AH, Susi P, Toivola H, Christensen A, Söderlund-Venermo M et al. 2016. Detection and monitoring of human bocavirus 1 infection by a new rapid antigen test. New Microbes New Infect 11:17–19
    [Google Scholar]
  103. 103. 
    Kols NI, Aatola H, Peltola V, Xu M, Nora-Krukle Z et al. 2019. Comparison of phenotypic and genotypic diagnosis of acute human bocavirus 1 infection in children. J. Clin. Virol. In press
    [Google Scholar]
  104. 104. 
    Moesker FM, van Kampen JJA, van der Eijik AA, van Rossum AMC, de Hoog M et al. 2015. Human bocavirus infection as a cause of severe acute respiratory tract infection in children. Clin. Microbiol. Infect. 964:e1–8
    [Google Scholar]
  105. 105. 
    Oikawa J, Ogita J, Ishiwada N, Okada T, Endo R, Ishiguro N 2009. Human bocavirus DNA detected in a boy with plastic bronchitis. Pediatr. Infect. Dis. J. 28:1035–36
    [Google Scholar]
  106. 106. 
    Ursic T, Steyer A, Kopriva S, Kalan G, Krivec U, Petrovec M 2011. Human bocavirus as the cause of a life-threatening infection. J. Clin. Microbiol. 49:1179–81
    [Google Scholar]
  107. 107. 
    Körner RM, Söderlund-Venermo M, van Koningsbruggen-Rietschel S, Kaiser R, Malecki M, Schildgen O 2011. Severe pneumonia in an infant caused by the human bocavirus, Germany. Emerg. Infect. Dis. 17:2303–5
    [Google Scholar]
  108. 108. 
    Edner N, Castillo-Rodas P, Falk L, Hedman K, Söderlund-Venermo M, Allander T 2012. Life-threatening respiratory tract disease with human bocavirus infection. J. Clin. Microbiol. 50:531–32
    [Google Scholar]
  109. 109. 
    Ursic T, Krivec U, Kalan G, Petrovec M 1015. Fatal human bocavirus infection in an 18-month-old child with chronic lung disease of prematurity. Pediatr. Infect. Dis. J. 34:111–12
    [Google Scholar]
  110. 110. 
    Eskola V, Xu M, Söderlund-Venermo M 2017. Severe lower respiratory tract infection with human bocavirus 1 in an infant. Pediatr. Infect. Dis. J. 36:1107–8
    [Google Scholar]
  111. 111. 
    Tabatabai J, Fakhiri J, Meyburg J, Linse K-P, Xu M et al. 2019. Severe human bocavirus 1 respiratory tract infection in an immunodeficient child with fatal outcome. Pediatr. Infect. Dis. J. In press. https://doi.org/10.1097/INF.0000000000002354
    [Crossref] [Google Scholar]
  112. 112. 
    Don M, Söderlund-Venermo M, Valent F, Lahtinen A, Hedman L et al. 2010. Serologically verified human bocavirus pneumonia in children. Pediatr. Pulmonol. 45:120–26
    [Google Scholar]
  113. 113. 
    Mitui MT, Tabib SB, Matsumoto T, Khanam W, Ahmed S et al. 2012. Detection of human bocavirus in the cerebrospinal fluid of children with encephalitis. Clin. Infect. Dis. 54:964–67
    [Google Scholar]
  114. 114. 
    Mori D, Ranawaka U, Yamada K, Tajindrajith S, Miya K et al. 2013. Human bocavirus in patients with encephalitis, Sri Lanka, 2009–2010. Emerg. Infect. Dis. 19:1859–62
    [Google Scholar]
  115. 115. 
    Yu JM, Chen QQ, Hao YX, Yu T, Zeng SZ et al. 2013. Identification of human bocaviruses in the cerebrospinal fluid of children hospitalized with encephalitis in China. J. Clin. Virol. 57:374–77
    [Google Scholar]
  116. 116. 
    Akturk H, Sik G, Salman N, Sutcu M, Tatli B et al. 2015. Atypical presentation of human bocavirus: severe respiratory tract infection complicated with encephalopathy. J. Med. Virol. 87:1831–38
    [Google Scholar]
  117. 117. 
    Kainulainen L, Waris M, Söderlund-Venermo M, Allander T, Hedman K, Ruuskanen O 2008. Hepatitis and human bocavirus primary infection in a child with T-cell deficiency. J. Clin. Microbiol. 46:4104–5
    [Google Scholar]
  118. 118. 
    Haytoglu Z, Canan O. 2017. Bocavirus viremia and hepatitis in an immunocompetent child. Balkan Med. J. 34:281–83
    [Google Scholar]
  119. 119. 
    Brebion A, Vanlieferinghen P, Déchelotte P, Boutry M, Peigue-Lafeuille H, Henquell C 2014. Fatal sub-acute myocarditis associated with human bocavirus 2 in a 13-month-old child. J. Clin. Microbiol. 52:1006–8
    [Google Scholar]
  120. 120. 
    Sharp CP, Lail A, Donfield S, Gomperts ED, Simmonds P 2012. Virologic and clinical features of primary infection with human parvovirus 4 in subjects with hemophilia: frequent transmission by virally inactivated clotting factor concentrates. Transfusion 52:1482–89
    [Google Scholar]
  121. 121. 
    Väisänen E, Lahtinen A, Hedman K, Söderlund-Venermo M 2014. A two-step real-time PCR assay for quantification and genotyping of human parvovirus 4 (PARV4). J. Virol. Methods 195:106–11
    [Google Scholar]
  122. 122. 
    Benjamin LA, Lewthwaite P, Vasanthapuram R, Zhao G, Sharp C et al. 2011. Human parvovirus 4 as potential cause of encephalitis in children, India. Emerg. Infect. Dis. 17:1484–87
    [Google Scholar]
  123. 123. 
    Prakas S, Jain A, Seth A, Singh AK, Jain B 2015. Complete genome sequences of two isolates of human parvovirus 4 from patients with acute encephalitis syndrome. Genome Announc 3:e01472–14
    [Google Scholar]
  124. 124. 
    Altay AK, Ocal M, Polat M, Kanik SY, Aktas AT et al. 2017. Multicenter investigation of bufavirus in the etiology of viral central nervous system infections of adults and children. Mikrobiyol. Bul. 51:191–94
    [Google Scholar]
  125. 125. 
    Anderson MJ, Jones SE, Fisher-Hoch SP, Lewis E, Hall SM et al. 1983. Human parvo virus, the cause of erythema infectiosum (fifth disease)?. Lancet 1:1378
    [Google Scholar]
  126. 126. 
    Anderson MJ, Higgins PG, Davis LR, Willman JS, Jones SE et al. 1985. Experimental parvoviral infection in humans. J. Infect. Dis. 152:257–65
    [Google Scholar]
  127. 127. 
    Anderson MJ. 1982. The emerging story of a human parvovirus-like agent. J. Hyg. Camb. 89:1–8
    [Google Scholar]
  128. 128. 
    Bihari C, Rastogi A, Saxena P, Rangegowda D, Chowdhury A et al. 2013. Parvovirus B19 associated hepatitis. Hepat. Res. Treat. 2013:472027
    [Google Scholar]
  129. 129. 
    Söderlund M, von Essen R, Haapasaari J, Kiistala U, Kiviluoto O, Hedman K 1997. Persistence of parvovirus B19 DNA in synovial membranes of young patients with and without chronic arthropathy. Lancet 349:1063–65
    [Google Scholar]
  130. 130. 
    Norja P, Hokynar K, Aaltonen L-M, Chen R, Ranki A et al. 2006. Bioportfolio: life-long persistence of variant and prototypic erythrovirus DNA genomes in human tissue. PNAS 103:7450–53
    [Google Scholar]
  131. 131. 
    Hokynar K, Norja P, Hedman K, Söderlund-Venermo M 2007. Tissue persistence and prevalence of parvovirus B19 types 1–3. Future Virol 2:377–88
    [Google Scholar]
  132. 132. 
    Grant JK, Yin NC, Zatoun AM, Waseem H, Hobbs JA 2009. Persistent adeno-associated virus 2 and parvovirus B19 sequences in post-mortem human cerebellum. Cerebellum 8:490–98
    [Google Scholar]
  133. 133. 
    Verdonschot J, Hazebroek M, Merken J, Debing Y, Dennert R et al. 2016. Relevance of cardiac parvovirus B19 in myocarditis and dilated cardiomyopathy: review of the literature. Europ. J. Heart Failure 18:1430–41
    [Google Scholar]
  134. 134. 
    Adamson-Small LA, Ignatovich IV, Laemmerhirt MG, Hobbs JA 2014. Persistent parvovirus B19 infection in non-erythroid tissues: possible role in the inflammatory and disease process. Virus Res 190:8–16
    [Google Scholar]
  135. 135. 
    Toppinen M, Perdomo M, Palo JU, Simmonds P, Lycett SJ et al. 2015. Bones hold the key to DNA virus history and epidemiology. Sci. Rep. 5:17226
    [Google Scholar]
  136. 136. 
    Santonja C, Santos-Briz A, Palmedo G, Kutzner H, Requena L 2017. Detection of human parvovirus B19 DNA in 22% of 1,815 cutaneous biopsies of a wide variety of dermatologic conditions suggests viral persistence after primary infection and casts doubts on its pathogenic significance. Br. J. Dermatol. 177:1060–65
    [Google Scholar]
  137. 137. 
    Söderlund-Venermo M. 2017. Clinical significance of parvovirus B19 DNA in cutaneous biopsies. Br. J. Dermatol. 177:900–1
    [Google Scholar]
  138. 138. 
    Pyöriä L, Toppinen M, Mäntylä E, Hedman L, Aaltonen LM et al. 2017. Extinct type of human parvovirus B19 persists in tonsillar B cells. Nat. Commun. 8:14930
    [Google Scholar]
  139. 139. 
    Schneider B, Fryer JF, Reber U, Fischer HP, Tolba RH et al. 2008. Persistence of novel human parvovirus PARV4 in liver tissue of adults. J. Med. Virol. 80:345–51
    [Google Scholar]
  140. 140. 
    Lu X, Gooding LR, Erdman DD 2008. Human bocavirus in tonsillar lymphocytes. Emerg. Infect. Dis. 14:1332–34
    [Google Scholar]
  141. 141. 
    Clément N, Battaglioli G, Jensen RL, Schnepp BC, Johnson PR et al. 2009. Prevalence of human bocavirus in human tonsils and adenoids. Emerg. Infect. Dis. 15:1149–50
    [Google Scholar]
  142. 142. 
    Norja P, Hedman L, Kantola K, Kemppainen K, Suvilehto J et al. 2012. Occurrence of human bocaviruses and parvovirus 4 in solid tissues. J. Med. Virol. 84:1267–73
    [Google Scholar]
  143. 143. 
    Kapoor A, Hornig M, Asokan A, Williams B, Henriquez JA et al. 2011. Bocavirus episome in infected human tissue contains non-identical termini. PLOS ONE 6:e21362
    [Google Scholar]
  144. 144. 
    Schildgen V, Malecki M, Tillmann RL, Brockmann M, Schildgen O 2013. The human bocavirus is associated with some lung and colorectal cancers and persists in solid tumors. PLOS ONE 8:e680200
    [Google Scholar]
  145. 145. 
    Abdel-Moneim A, El-Fol HA, Kamel MM, Soliman AS, Mahdi EA et al. 2016. Screening of human bocavirus in surgically excised cancer specimens. Arch. Virol. 161:2095–102
    [Google Scholar]
  146. 146. 
    Höpken M, Förster I, Maune S, Brockmann M, Schildgen O, Schildgen V 2018. Association of the human bocavirus with tonsil squamous cell carcinomas. Front. Microbiol. 9:2450
    [Google Scholar]
  147. 147. 
    Deng X, Zou W, Xiong M, Wang Z, Engelhardt JF et al. 2017. Human parvovirus infection of human airway epithelia induces pyroptotic cell death by inhibiting apoptosis. J. Virol. 91:e01533–17
    [Google Scholar]
  148. 148. 
    Mollerup S, Fridholm H, Vinner L, Kjartansdottir KR, Friis-Nielsen J et al. 2017. Cutavirus in cutaneous malignant melanoma. Emerg. Infect. Dis. 23:363–65
    [Google Scholar]
  149. 149. 
    Kreuter A, Nasserani N, Tigges C, Oellig F, Silling S et al. 2018. Cutavirus in primary cutaneous B- and T-cell lymphoma. JAMA Dermatol 154:965–67
    [Google Scholar]
  150. 150. 
    Mirvish JJ, Pomerantz RG, Falo LD Jr., Geskin LJ 2013. Role of infectious agents in cutaneous T-cell lymphoma: facts and controversies. Clin. Dermatol. 31:423–31
    [Google Scholar]
  151. 151. 
    Nüesch J, LaCroix J, Marchini A, Rommelaere J 2012. Molecular pathways: rodent parvoviruses—mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 18:3516–23
    [Google Scholar]
  152. 152. 
    Kishore J, Kishor D. 2014. Can parvovirus B19 infection be naturally oncolytic: clinical findings raise such a possibility in leukaemic children. Indian J. Med. Res. 139:952–53
    [Google Scholar]
  153. 153. 
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:131605–12
    [Google Scholar]
  154. 154. 
    DeLano WL. 2002. The PyMOL molecular graphics system. Proteins 30:442–54
    [Google Scholar]
/content/journals/10.1146/annurev-virology-092818-015803
Loading
/content/journals/10.1146/annurev-virology-092818-015803
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error