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Chapter 30 : Human Parvoviruses

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Abstract:

Parvoviruses have been isolated from a wide range of animals, including mammals, birds, insects, crustaceans, and reptiles. These viruses tend to be species-specific and can cause a variety of serious diseases in their host species (1). The first parvoviruses isolated from humans were adeno-associated parvoviruses, which have not yet been linked with disease. Until recently the only parvovirus associated with human disease was human parvovirus B19 (B19V), which was fortuitously identified in 1975 during an evaluation of tests for hepatitis B virus antigens (2). B19V has been associated with erythema infectiosum, transient aplastic crisis, chronic anemia in patients with impaired immune systems, hydrops fetalis, and purportedly a number of other conditions (3). Seven additional parvoviruses have recently been detected in humans by molecular screening for new sequences, including human bocavirus (HBoV)1–4, tetraparvovirus (PARV4), bufavirus (BuV), and tusavirus (TuV) (4–9). HBoV1 causes acute respiratory illness (10) and, as with HBoV2 and 3, possibly also encephalitis (11). The other recently discovered human parvoviruses are yet to be associated with human disease.

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Figures

Image of FIGURE 1
FIGURE 1

Neighbor joining phylogenetic tree derived from ORF1 (nonstructural protein) amino acid sequences obtained from GenBank and used by ICTV to classify parvoviruses ( ). Subfamilies and shown as gray circles. For simplicity, only one representative member of the is shown and only genera of the with members known to infect humans are shown as yellow circles (, , and , genera are therefore excluded). Representative human parvoviruses (in red), putative human viruses (in blue), and prototype viruses when not human (in black) are shown within each genus. AA, amino acid; AaeDV1, densovirus 1; AAV1, AAV2, AAV5, adeno-associated viruses 1, 2, 5; B19V1–3, parvovirus B19 genotypes 1–3; BPV1, bovine parvovirus 1; BuV1–3, bufavirus genotypes 1–3; HBoV1–4, human bocavirueses 1–4; MVM, minute virus of mice; PARV4 1–3, tetraparvovirus genotypes 1–3; TuV1, tusavirus genotype 1.

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 2
FIGURE 2

Electron micrograph (X170,000) of B19V empty particles in a serum specimen from a patient with transient aplastic crisis. Courtesy of G. William Gary, CDC, Atlanta, GA.

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 3
FIGURE 3

Schematic of B19 mRNA produced in erythroid progenitor cells. The thin line represents introns and the heavy line represents the nontranslated portion of exons. The filled box represents translated portions of exons. The numbers below the line indicate the start or end of the respective exon. All mRNAs are initiated at the same promotor (P6). The NS protein (first mRNA) is in one reading frame; the 7.5 kDa, VP1, and VP2 proteins are in a second reading frame (-1 relative to the NS protein); and the 11.0 kDa protein is in the third reading frame. Based on data from references and .

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 4
FIGURE 4

Rates of B19V IgG antibody positivity by age. Adapted from reference .

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 5
FIGURE 5

(A) Hematoxylin and eosin stain of bone marrow from patient with B19V infection. Note prominent intranuclear inclusions (arrows). (B) Immunostaining of B19V antigens in bone marrow (immunoalkaline phosphatase stain, naphthol fast red substrate with light hematoxylin counterstain). Original magnification of both images, X630. Panels courtesy of Wun-Ju Shieh, CDC, Atlanta, GA.

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 6
FIGURE 6

Pathophysiology of parvovirus B19 infection. Inoculation of normal subjects and natural infection resulted in fifth disease (Panel A; study reported by Anderson et al. [ ]). A two-phase illness was produced under control conditions; most subjects noted only the typical rash, joint symptoms, or both, corresponding to the appearance of specific antiviral antibodies. Reticulocytopenia occurs during viremia, but hemoglobin levels do not decline below normal values. H denotes hemoglobin, and R reticulocytes. Transient aplastic crisis occurs in patients with underlying hemolysis or erythroid stress who are infected with parvovirus B19 (Panel B; study reported by Saarinen et al. [ ]). Cessation of erythropoiesis causes severe anemia, because of the higher demand for red cells. Chronic pure red-cell aplasia is due to persistent infection (Panel C; study reported by Kurtzman et al. [ ]). Anemia persists because of the failure of the humoral immune response to clear parvovirus B19. Reprinted from reference .

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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Image of FIGURE 7
FIGURE 7

Erythema infectiosum (fifth disease) associated with parvovirus B19.

Citation: Söderlund-Venermo M, Brown K, Erdman D. 2017. Human Parvoviruses, p 679-699. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch30
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References

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1. Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ, Qiu J, Söderlund-Venermo M, Tattersall P, Tijssen P, Gatherer D, Davison AJ . 2014. The family Parvoviridae. Arch Virol 159 : 1239 1247.[PubMed]
2. Cossart YE, Field AM, Cant B, Widdows D . 1975. Parvovirus-like particles in human sera. Lancet 1 : 72 73.[PubMed]
3. Young NS, Brown KE . 2004. Parvovirus B19. N Engl J Med 350 : 586 597.[PubMed]
4. 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. Proc Natl Acad Sci USA 102 : 12891 12896.[PubMed]
5. 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.[PubMed]
6. 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 8236.[PubMed]
7. Kapoor A, Slikas E, Simmonds P, Chieochansin T, Naeem A, Shaukat S, Alam MM, Sharif S, Angez M, Zaidi S, Delwart E . 2009. A newly identified bocavirus species in human stool. J Infect Dis 199 : 196 200.[PubMed]
8. Phan TG, Vo NP, Bonkoungou IJ, Kapoor A, Barro N, O'Ryan M, Kapusinszky B, Wang C, Delwart E . 2012. Acute diarrhea in West African children: diverse enteric viruses and a novel parvovirus genus. J Virol 86 : 11024 11030.[PubMed]
9. Phan TG, Sdiri-Loulizi K, Aouni M, Ambert-Balay K, Pothier P, Deng X, Delwart E . 2014. New parvovirus in child with unexplained diarrhea, Tunisia. Emerg Infect Dis 20 : 1911 1913.[PubMed]
10. 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.[PubMed]
11. Mori D, Ranawaka U, Yamada K, Rajindrajith S, Miya K, Perera HK, Matsumoto T, Dassanayake M, Mitui MT, Mori H, Nishizono A, Söderlund-Venermo M, Ahmed K . 2013. Human bocavirus in patients with encephalitis, Sri Lanka, 2009–2010. Emerg Infect Dis 19 : 1859 1862.[PubMed]
12. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X, Wilson JM . 2004. Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 78 : 6381 6388.[PubMed]
13. Warrington KH Jr, Herzog RW . 2006. Treatment of human disease by adeno-associated viral gene transfer. Hum Genet 119 : 571 603.[PubMed]
14. Ekman A, Hokynar K, Kakkola L, Kantola K, Hedman L, Bondén H, Gessner M, Aberham C, Norja P, Miettinen S, Hedman K, Söderlund-Venermo M . 2007. Biological and immunological relations among human parvovirus B19 genotypes 1 to 3. J Virol 81 : 6927 6935[PubMed].
15. Hokynar K, Söderlund-Venermo M, Pesonen M, Ranki A, Kiviluoto O, Partio EK, Hedman K . 2002. A new parvovirus genotype persistent in human skin. Virology 302 : 224 228.[PubMed]
16. Nguyen QT, Sifer C, Schneider V, Allaume X, Servant A, Bernaudin F, Auguste V, Garbarg-Chenon A . 1999. Novel human erythrovirus associated with transient aplastic anemia. J Clin Microbiol 37 : 2483 2487.[PubMed]
17. Nguyen QT, Wong S, Heegaard ED, Brown KE . 2002. Identification and characterization of a second novel human erythrovirus variant, A6. Virology 301 : 374 380.[PubMed]
18. Servant A, Laperche S, Lallemand F, Marinho V, De Saint Maur G, Meritet JF, Garbarg-Chenon A . 2002. Genetic diversity within human erythroviruses: identification of three genotypes. J Virol 76 : 9124 9134.[PubMed]
19. Norja P, Hokynar K, Aaltonen LM, Chen R, Ranki A, Partio EK, Kiviluoto O, Davidkin I, Leivo T, Eis-Hübinger AM, Schneider B, Fischer HP, Tolba R, Vapalahti O, Vaheri A, Söderlund-Venermo M, Hedman K . 2006. Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc Natl Acad Sci USA 103 : 7450 7453.[PubMed]
20. Candotti D, Etiz N, Parsyan A, Allain JP . 2004. Identification and characterization of persistent human erythrovirus infection in blood donor samples. J Virol 78 : 12169 12178[PubMed].
21. Fryer JF, Delwart E, Bernardin F, Tuke PW, Lukashov VV, Baylis SA . 2007. Analysis of two human parvovirus PARV4 genotypes identified in human plasma for fractionation. J Gen Virol 88 : 2162 2167.[PubMed]
22. Matthews PC, Sharp CP, Malik A, Gregory WF, Adland E, Jooste P, Goulder PJ, Simmonds P, Klenerman P . 2015. Human parvovirus 4 infection among mothers and children in South Africa. Emerg Infect Dis 21 : 713 715.[PubMed]
23. Panning M, Kobbe R, Vollbach S, Drexler JF, Adjei S, Adjei O, Drosten C, May J, Eis-Hübinger AM . 2010. Novel human parvovirus 4 genotype 3 in infants, Ghana. Emerg Infect Dis 16 : 1143 1146.[PubMed]
24. Simmonds P, Douglas J, Bestetti G, Longhi E, Antinori S, Parravicini C, Corbellino M . 2008. A third genotype of the human parvovirus PARV4 in sub-Saharan Africa. J Gen Virol 89 : 2299 2302.[PubMed]
25. Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L, Sethabutr O, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser J, Bartkus J, Delwart E . 2010. Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201 : 1633 1643.[PubMed]
26. Kapoor A, Mehta N, Esper F, Poljsak-Prijatelj M, Quan PL, Qaisar N, Delwart E, Lipkin WI . 2010. Identification and characterization of a new bocavirus species in gorillas. PLoS One 5 : e11948.[PubMed]
27. Yahiro T, Wangchuk S, Tshering K, Bandhari P, Zangmo S, Dorji T, Tshering K, Matsumoto T, Nishizono A, Söderlund-Venermo M, Ahmed K . 2014. Novel human bufavirus genotype 3 in children with severe diarrhea, Bhutan. Emerg Infect Dis 20 : 1037 1039.[PubMed]
28. Cecchini S, Negrete A, Virag T, Graham BS, Cohen JI, Kotin RM . 2009. Evidence of prior exposure to human bocavirus as determined by a retrospective serological study of 404 serum samples from adults in the United States. Clin Vaccine Immunol 16 : 597 604.[PubMed]
29. Zou W, Cheng F, Shen W, Engelhardt JF, Yan Z, Qiu J . Nonstructural protein NP1 of human bocavirus 1 plays a critical role in the expression of viral capsid proteins. J Virol, in press.
30. Halder S, Ng R, Agbandje-McKenna M . 2012. Parvoviruses: structure and infection. Future Virol 7 : 253 278.
31. Cotmore SF, Tattersall P, . 2006. Structure and organization of the viral genome, p 73 94. In Kerr JR, Cotmore SF, Bloom ME, Linden RM, Parrish CR (ed), Parvoviruses. Hodder Arnold, London.
32. Sun Y, Chen AY, Cheng F, Guan W, Johnson FB, Qiu J . 2009. Molecular characterization of infectious clones of the minute virus of canines reveals unique features of bocaviruses. J Virol 83 : 3956 3967.[PubMed]
33. Böhmer A, Schildgen V, Lüsebrink J, Ziegler S, Tillmann RL, Kleines M, Schildgen O . 2009. Novel application for isothermal nucleic acid sequence-based amplification (NASBA). J Virol Methods 158 : 199 201.[PubMed]
34. Ozawa K, Ayub J, Hao YS, Kurtzman G, Shimada T, Young N . 1987. Novel transcription map for the B19 (human) pathogenic parvovirus. J Virol 61 : 2395 2406.[PubMed]
35. Luo W, Astell CR . 1993. A novel protein encoded by small RNAs of parvovirus B19. Virology 195 : 448 455.[PubMed]
36. Ozawa K, Ayub J, Young N . 1988. Functional mapping of the genome of the B19 (human) parvovirus by in vitro translation after negative hybrid selection. J Virol 62 : 2508 2511.[PubMed]
37. St Amand J, Astell CR . 1993. Identification and characterization of a family of 11-kDa proteins encoded by the human parvovirus B19. Virology 192 : 121 131.[PubMed]
38. Modrow S . 2006. Parvovirus B19: the causative agent of dilated cardiomyopathy or a harmless passenger of the human myocard? Ernst Schering Res Found Workshop 2006 : 63 82.[PubMed]
39. Chen AY, Cheng F, Lou S, Luo Y, Liu Z, Delwart E, Pintel D, Qiu J . 2010. Characterization of the gene expression profile of human bocavirus. Virology 403 : 145 154.[PubMed]
40. Ozawa K, Young N . 1987. Characterization of capsid and noncapsid proteins of B19 parvovirus propagated in human erythroid bone marrow cell cultures. J Virol 61 : 2627 2630.[PubMed]
41. Wong S, Momoeda M, Field A, Kajigaya S, Young NS . 1994. Formation of empty B19 parvovirus capsids by the truncated minor capsid protein. J Virol 68 : 4690 4694.[PubMed]
42. Kajigaya S, Fujii H, Field A, Anderson S, Rosenfeld S, Anderson LJ, Shimada T, Young NS . 1991. Self-assembled B19 parvovirus capsids, produced in a baculovirus system, are antigenically and immunogenically similar to native virions. Proc Natl Acad Sci USA 88 : 4646 4650.[PubMed]
43. Cotmore SF, Tattersall P . 2007. Parvoviral host range and cell entry mechanisms. Adv Virus Res 70 : 183 232.[PubMed]
44. Zádori Z, Szelei J, Lacoste MC, Li Y, Gariépy S, Raymond P, Allaire M, Nabi IR, Tijssen P . 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 1 : 291 302.[PubMed]
45. Brown KE, Anderson SM, Young NS . 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262 : 114 117.[PubMed]
46. Munakata Y, Saito-Ito T, Kumura-Ishii K, Huang J, Kodera T, Ishii T, Hirabayashi Y, Koyanagi Y, Sasaki T . 2005. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 106 : 3449 3456.[PubMed]
47. Weigel-Kelley KA, Yoder MC, Srivastava A . 2001. Recombinant human parvovirus B19 vectors: erythrocyte P antigen is necessary but not sufficient for successful transduction of human hematopoietic cells. J Virol 75 : 4110 4116.[PubMed]
48. Weigel-Kelley KA, Yoder MC, Srivastava A . 2003. α5β1 integrin as a cellular coreceptor for human parvovirus B19: requirement of functional activation of β1 integrin for viral entry. Blood 102 : 3927 3933.[PubMed]
49. 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 13167.[PubMed]
50. Pillet S, Le Guyader N, Hofer T, NguyenKhac F, Koken M, Aubin JT, Fichelson S, Gassmann M, Morinet F . 2004. Hypoxia enhances human B19 erythrovirus gene expression in primary erythroid cells. Virology 327 : 1 7.[PubMed]
51. Chen AY, Kleiboeker S, Qiu J . 2011. Productive parvovirus B19 infection of primary human erythroid progenitor cells at hypoxia is regulated by STAT5A and MEK signaling but not HIFα. PLoS Pathog 7 : e1002088.[PubMed]
52. Lou S, Luo Y, Cheng F, Huang Q, Shen W, Kleiboeker S, Tisdale JF, Liu Z, Qiu J . 2012. Human parvovirus B19 DNA replication induces a DNA damage response that is dispensable for cell cycle arrest at phase G2/M. J Virol 86 : 10748 10758.[PubMed]
53. Luo Y, Qiu J . 2013. Parvovirus infection–induced DNA damage response. Future Virol 8 : 245 257.[PubMed]
54. 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 12 : e1005399.[PubMed]
55. Tattersall P, Ward DC . 1976. Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263 : 106 109.[PubMed]
56. Chen KC, Shull BC, Moses EA, Lederman M, Stout ER, Bates RC . 1986. Complete nucleotide sequence and genome organization of bovine parvovirus. J Virol 60 : 1085 1097.[PubMed]
57. Brown KE, Liu Z, Gallinella G, Wong S, Mills IP, O'Sullivan MG . 2004. Simian parvovirus infection: a potential zoonosis. J Infect Dis 190 : 1900 1907.[PubMed]
58. Kemenesi G, Dallos B, Görföl T, Estók P, Boldogh S, Kurucz K, Oldal M, Marton S, Bányai K, Jakab F . 2015. Genetic diversity and recombination within bufaviruses: detection of a novel strain in Hungarian bats. Infect Genet Evol 33 : 288 292.[PubMed]
59. Sharp CP, LeBreton M, Kantola K, Nana A, Diffo JD, Djoko CF, Tamoufe U, Kiyang JA, Babila TG, Ngole EM, Pybus OG, Delwart E, Delaporte E, Peeters M, Söderlund-Venermo M, Hedman K, Wolfe ND, Simmonds P . 2010. Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild. J Virol 84 : 10289 10296.[PubMed]
60. Green SW, Malkovska I, O'Sullivan MG, Brown KE . 2000. Rhesus and pig-tailed macaque parvoviruses: identification of two new members of the erythrovirus genus in monkeys. Virology 269 : 105 112.[PubMed]
61. O'Sullivan MG, Anderson DK, Goodrich JA, Tulli H, Green SW, Young NS, Brown KE . 1997. Experimental infection of cynomolgus monkeys with simian parvovirus. J Virol 71 : 4517 4521.[PubMed]
62. Ozawa K, Kurtzman G, Young N . 1986. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233 : 883 886.[PubMed]
63. Komatsu N, Nakauchi H, Miwa A, Ishihara T, Eguchi M, Moroi M, Okada M, Sato Y, Wada H, Yawata Y, Suda T, Miura Y . 1991. Establishment and characterization of a human leukemic cell line with megakaryocytic features: dependency on granulocyte-macrophage colony-stimulating factor, interleukin 3, or erythropoietin for growth and survival. Cancer Res 51 : 341 348.[PubMed]
64. Miyagawa E, Yoshida T, Takahashi H, Yamaguchi K, Nagano T, Kiriyama Y, Okochi K, Sato H . 1999. Infection of the erythroid cell line, KU812Ep6 with human parvovirus B19 and its application to titration of B19 infectivity. J Virol Methods 83 : 45 54.[PubMed]
65. Pillet S, Le Guyader N, Hofer T, NguyenKhac F, Koken M, Aubin JT, Fichelson S, Gassmann M, Morinet F . 2004. Hypoxia enhances human B19 erythrovirus gene expression in primary erythroid cells. Virology 327 : 1 7.[PubMed]
66. Guan W, Wong S, Zhi N, Qiu J . 2009. The genome of human parvovirus B19 can replicate in nonpermissive cells with the help of adenovirus genes and produces infectious virus. J Virol 83 : 9541 9553.[PubMed]
67. Berns K, Parrish CR, . 2006. Parvoviridae, p. 2437 2477. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Reizman B,, and Straus SE (ed), Fields Virology, 5th ed, vol. 2. Wolters Kluwer, Lippincott Williams & Wilkins, Philadelphia, PA.
68. Dijkman R, Koekkoek SM, Molenkamp R, Schildgen O, van der Hoek L . 2009. Human bocavirus can be cultured in differentiated human airway epithelial cells. J Virol 83 : 7739 7748.[PubMed]
69. Huang Q, Deng X, Yan Z, Cheng F, Luo Y, Shen W, Lei-Butters DC, Chen AY, Li Y, Tang L, Söderlund-Venermo M, Engelhardt JF, Qiu J . 2012. Establishment of a reverse genetics system for studying human bocavirus in human airway epithelia. PLoS Pathog 8 : e1002899.[PubMed]
70. Sattar SA, Springthorpe VS, Karim Y, Loro P . 1989. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect 102 : 493 505.[PubMed]
71. Santagostino E, Mannucci PM, Gringeri A, Azzi A, Morfini M, Musso R, Santoro R, Schiavoni M . 1997. Transmission of parvovirus B19 by coagulation factor concentrates exposed to 100 degrees C heat after lyophilization. Transfusion 37 : 517 522.[PubMed]
72. Hattori S, Yunoki M, Tsujikawa M, Urayama T, Tachibana Y, Yamamoto I, Yamamoto S, Ikuta K . 2007. Variability of parvovirus B19 to inactivation by liquid heating in plasma products. Vox Sang 92 : 121 124.[PubMed]
73. Cohen BJ, Buckley MM . 1988. The prevalence of antibody to human parvovirus B19 in England and Wales. J Med Microbiol 25 : 151 153.[PubMed]
74. Jensen IP, Thorsen P, Jeune B, Møller BR, Vestergaard BF . 2000. An epidemic of parvovirus B19 in a population of 3,596 pregnant women: a study of sociodemographic and medical risk factors. BJOG 107 : 637 643.[PubMed]
75. Vyse AJ, Andrews NJ, Hesketh LM, Pebody R . 2007. The burden of parvovirus B19 infection in women of childbearing age in England and Wales. Epidemiol Infect 135 : 1354 1362.[PubMed]
76. 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 1784.[PubMed]
77. Smits SL, Schapendonk CM, van Beek J, Vennema H, Schürch AC, Schipper D, Bodewes R, Haagmans BL, Osterhaus AD, Koopmans MP . 2014. New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg Infect Dis 20 : 1218 1222.[PubMed]
78. Väisänen E, Kuisma I, Phan TG, Delwart E, Lappalainen M, Tarkka E, Hedman K, Söderlund-Venermo M . 2014. Bufavirus in feces of patients with gastroenteritis, Finland. Emerg Infect Dis 20 : 1077 1079.[PubMed]
79. Mossong J, Hens N, Friederichs V, Davidkin I, Broman M, Litwinska B, Siennicka J, Trzcinska A, Van Damme P, Beutels P, Vyse A, Shkedy Z, Aerts M, Massari M, Gabutti G . 2008. Parvovirus B19 infection in five European countries: seroepidemiology, force of infection and maternal risk of infection. Epidemiol Infect 136 : 1059 1068.[PubMed]
80. Melegaro A, Jit M, Gay N, Zagheni E, Edmunds WJ . 2011. What types of contacts are important for the spread of infections? using contact survey data to explore European mixing patterns. Epidemics 3 : 143 151.[PubMed]
81. Tolfvenstam T, Enbom M, Ghebrekidan H, Rudén U, Linde A, Grandien M, Wahren B . 2000. Seroprevalence of viral childhood infections in Eritrea. J Clin Virol 16 : 49 54.[PubMed]
82. Wildig J, Michon P, Siba P, Mellombo M, Ura A, Mueller I, Cossart Y . 2006. Parvovirus B19 infection contributes to severe anemia in young children in Papua New Guinea. J Infect Dis 194 : 146 153.[PubMed]
83. de Freitas RB, Wong D, Boswell F, de Miranda MF, Linhares AC, Shirley J, Desselberger U . 1990. Prevalence of human parvovirus (B19) and rubella virus infections in urban and remote rural areas in northern Brazil. J Med Virol 32 : 203 208.[PubMed]
84. Ke L, He M, Li C, Liu Y, Gao L, Yao F, Li J, Bi X, Lv Y, Wang J, Hirsch ML, Li W . 2011. The prevalence of human parvovirus B19 DNA and antibodies in blood donors from four Chinese blood centers. Transfusion 51 : 1909 1918.[PubMed]
85. Schwarz TF, Gürtler LG, Zoulek G, Deinhardt F, Roggendorf M . 1989. Seroprevalence of human parvovirus B19 infection in Sao Tomé and Principe, Malawi and Mascarene Islands. Zentralbl Bakteriol 271 : 231 236.[PubMed]
86. Chorba T, Coccia P, Holman RC, Tattersall P, Anderson LJ, Sudman J, Young NS, Kurczynski E, Saarinen UM, Moir R, Lawrence DN, Jason JM, Evatt B . 1986. The role of parvovirus B19 in aplastic crisis and erythema infectiosum (fifth disease). J Infect Dis 154 : 383 393.[PubMed]
87. Plummer FA, Hammond GW, Forward K, Sekla L, Thompson LM, Jones SE, Kidd IM, Anderson MJ . 1985. An erythema infectiosum–like illness caused by human parvovirus infection. N Engl J Med 313 : 74 79[PubMed].
88. Woolf AD, Campion GV, Chishick A, Wise S, Cohen BJ, Klouda PT, Caul O, Dieppe PA . 1989. Clinical manifestations of human parvovirus B19 in adults. Arch Intern Med 149 : 1153 1156.[PubMed]
89. Gillespie SM, Cartter ML, Asch S, Rokos JB, Gary GW, Tsou CJ, Hall DB, Anderson LJ, Hurwitz ES . 1990. Occupational risk of human parvovirus B19 infection for school and day-care personnel during an outbreak of erythema infectiosum. JAMA 263 : 2061 2065.[PubMed]
90. Cartter ML, Farley TA, Rosengren S, Quinn DL, Gillespie SM, Gary GW, Hadler JL . 1991. Occupational risk factors for infection with parvovirus B19 among pregnant women. J Infect Dis 163 : 282 285.[PubMed]
91. Tuckerman JG, Brown T, Cohen BJ . 1986. Erythema infectiosum in a village primary school: clinical and virological studies. J R Coll Gen Pract 36 : 267 270.[PubMed]
92. Anderson MJ, Higgins PG, Davis LR, Willman JS, Jones SE, Kidd IM, Pattison JR, Tyrrell DAJ . 1985. Experimental parvoviral infection in humans. J Infect Dis 152 : 257 265.[PubMed]
93. Kantola K, Hedman L, Tanner L, Simell V, Mäkinen M, Partanen J, Sadeghi M, Veijola R, Knip M, Ilonen J, Hyöty H, Toppari J, Simell O, Hedman K, Söderlund-Venermo M . 2015. B-cell responses to human bocaviruses 1–4: new insights from a childhood follow-up study. PLoS One 10 : e0139096.[PubMed]
94. Kantola K, Hedman L, Arthur J, Alibeto A, Delwart E, Jartti T, Ruuskanen O, Hedman K, Söderlund-Venermo M . 2011. Seroepidemiology of human bocaviruses 1–4. J Infect Dis 204 : 1403 1412.[PubMed]
95. 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 3108.[PubMed]
96. Erles K, Sebökovà P, Schlehofer JR . 1999. Update on the prevalence of serum antibodies (IgG and IgM) to adeno-associated virus (AAV). J Med Virol 59 : 406 411.[PubMed]
97. Sharp CP, Lail A, Donfield S, Simmons R, Leen C, Klenerman P, Delwart E, Gomperts ED, Simmonds P . 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 1125.[PubMed]
98. Simmons R, Sharp C, McClure CP, Rohrbach J, Kovari H, Frangou E, Simmonds P, Irving W, Rauch A, Bowness P, Klenerman P Swiss HIV Cohort Study . 2012. Parvovirus 4 infection and clinical outcome in high-risk populations. J Infect Dis 205 : 1816 1820.[PubMed]
99. Lahtinen A, Kivelä P, Hedman L, Kumar A, Kantele A, Lappalainen M, Liitsola K, Ristola M, Delwart E, Sharp C, Simmonds P, Söderlund-Venermo M, Hedman K . 2011. Serodiagnosis of primary infections with human parvovirus 4, Finland. Emerg Infect Dis 17 : 79 82.[PubMed]
100. Sharp CP, Vermeulen M, Nébié Y, Djoko CF, LeBreton M, Tamoufe U, Rimoin AW, Kayembe PK, Carr JK, Servant-Delmas A, Laperche S, Harrison GL, Pybus OG, Delwart E, Wolfe ND, Saville A, Lefrère JJ, Simmonds P . 2010. Changing epidemiology of human parvovirus 4 infection in sub-Saharan Africa. Emerg Infect Dis 16 : 1605 1607.[PubMed]
101. Tong R, Shen L, Yin W, Zhou W, Lu J, Zheng M, Bi S, Lou Y, Tan W . 2013. Prevalence of human parvovirus B19, bocavirus, and PARV4 in blood samples from the general population of China and lack of a correlation between parvovirus and hepatitis B co-infection. PLoS One 8 : e64391.[PubMed]
102. Altay A, Yahiro T, Bozdayi G, Matsumoto T, Sahin F, Ozkan S, Nishizono A, Söderlund-Venermo M, Ahmed K . 2015. Bufavirus genotype 3 in Turkish children with severe diarrhoea. Clin Microbiol Infect 21 : 965.e1 965.e4; Epub ahead of print.[PubMed]
103. Health Protection Agency . 2012. Increased parvovirus B19 activity in England and Wales. Health Protection Report 6 : 23. www.gov.uk/guidance/parvovirus-b19
104. Kelly HA, Siebert D, Hammond R, Leydon J, Kiely P, Maskill W . 2000. The age-specific prevalence of human parvovirus immunity in Victoria, Australia compared with other parts of the world. Epidemiol Infect 124 : 449 457.[PubMed]
105. Naides SJ . 1988. Erythema infectiosum (fifth disease) occurrence in Iowa. Am J Public Health 78 : 1230 1231.[PubMed]
106. 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 1352.[PubMed]
107. Arnold JC, Singh KK, Spector SA, Sawyer MH . 2006. Human bocavirus: prevalence and clinical spectrum at a children's hospital. Clin Infect Dis 43 : 283 288.[PubMed]
108. Bastien N, Chui N, Robinson JL, Lee BE, Dust K, Hart L, Li Y . 2007. Detection of human bocavirus in Canadian children in a 1-year study. J Clin Microbiol 45 : 610 613.[PubMed]
109. Fry AM, Lu X, Chittaganpitch M, Peret T, Fischer J, Dowell SF, Anderson LJ, Erdman D, Olsen SJ . 2007. Human bocavirus: a novel parvovirus epidemiologically associated with pneumonia requiring hospitalization in Thailand. J Infect Dis 195 : 1038 1045.[PubMed]
110. Kesebir D, Vazquez M, Weibel C, Shapiro ED, Ferguson D, Landry ML, Kahn JS . 2006. Human bocavirus infection in young children in the United States: molecular epidemiological profile and clinical characteristics of a newly emerging respiratory virus. J Infect Dis 194 : 1276 1282.[PubMed]
111. Lau SK, Yip CC, Que TL, Lee RA, Au-Yeung RK, Zhou B, So LY, Lau YL, Chan KH, Woo PC, Yuen KY . 2007. Clinical and molecular epidemiology of human bocavirus in respiratory and fecal samples from children in Hong Kong. J Infect Dis 196 : 986 993.[PubMed]
112. Meriluoto M, Hedman L, Tanner L, Simell V, Mäkinen M, Simell S, Mykkänen J, Korpelainen J, Ruuskanen O, Ilonen J, Knip M, Simell O, Hedman K, Söderlund-Venermo M . 2012. Association of human bocavirus 1 infection with respiratory disease in childhood follow-up study, Finland. Emerg Infect Dis 18 : 264 271.[PubMed]
113. Anderson MJ, Davis LR, Jones SE, Pattison JR, Serjeant GR . 1982. The development and use of an antibody capture radioimmunoassay for specific IgM to a human parvovirus–like agent. J Hyg (Lond) 88 : 309 324.[PubMed]
114. Azzi A, Morfini M, Mannucci PM . 1999. The transfusion-associated transmission of parvovirus B19. Transfus Med Rev 13 : 194 204.[PubMed]
115. Brown KE, Young NS, Alving BM, Barbosa LH . 2001. Parvovirus B19: implications for transfusion medicine. Summary of a workshop. Transfusion 41 : 130 135.[PubMed]
116. Williams MD, Cohen BJ, Beddall AC, Pasi KJ, Mortimer PP, Hill FG . 1990. Transmission of human parvovirus B19 by coagulation factor concentrates. Vox Sang 58 : 177 181.[PubMed]
117. Shneerson JM, Mortimer PP, Vandervelde EM . 1980. Febrile illness due to a parvovirus. BMJ 280 : 1580.[PubMed]
118. Schmidt M, Themann A, Drexler C, Bayer M, Lanzer G, Menichetti E, Lechner S, Wessin D, Prokoph B, Allain JP, Seifried E, Hourfar MK . 2007. Blood donor screening for parvovirus B19 in Germany and Austria. Transfusion 47 : 1775 1782.[PubMed]
119. Nübling CM, Daas A, Buchheit KH . 2004. Collaborative study for establishment of a European Pharmacopoei Biological Reference Preparation (BRP) for B19 virus DNA testing of plasma pools by nucleic acid amplification technique. Pharmeur Bio 2003 : 27 34.[PubMed]
120. Tabor E, Epstein JS . 2002. NAT screening of blood and plasma donations: evolution of technology and regulatory policy. Transfusion 42 : 1230 1237.[PubMed]
121. Dowell SF, Török TJ, Thorp JA, Hedrick J, Erdman DD, Zaki SR, Hinkle CJ, Bayer WL, Anderson LJ . 1995. Parvovirus B19 infection in hospital workers: community or hospital acquisition? J Infect Dis 172 : 1076 1079.[PubMed]
122. García-Tapia AM, Fernández-Gutiérrez del Alamo C, Girón JA, Mira J, de la Rubia F, Martínez-Rodríguez A, Martín-Reina MV, López-Caparrós R, Cáliz R, Caballero MS, Bascuñana A . 1995. The spectrum of parvovirus B19 infection: analysis of an outbreak of 43 cases in Cadiz, Spain. Clin Infect Dis 21 : 1424 1430.[PubMed]
123. Miyamoto K, Ogami M, Takahashi Y, Mori T, Akimoto S, Terashita H, Terashita T . 2000. Outbreak of human parvovirus B19 in hospital workers. J Hosp Infect 45 : 238 241.[PubMed]
124. Seng C, Watkins P, Morse D, Barrett SP, Zambon M, Andrews N, Atkins M, Hall S, Lau YK, Cohen BJ . 1994. Parvovirus B19 outbreak on an adult ward. Epidemiol Infect 113 : 345 353.[PubMed]
125. Garner JS and The Hospital Infection Control Practices Advisory Committee . 1996. Guideline for isolation precautions in hospitals, 2nd ed., part 2. Rationale and recommendations. Infect Control Hospital Epidemiol 17 : 53 80.
126. Enders M, Weidner A, Enders G . 2007. Current epidemiological aspects of human parvovirus B19 infection during pregnancy and childhood in the western part of Germany. Epidemiol Infect 135 : 563 569.[PubMed]
127. Koch WC, Adler SP . 1989. Human parvovirus B19 infections in women of childbearing age and within families. Pediatr Infect Dis J 8 : 83 87.[PubMed]
128. van Gessel PH, Gaytant MA, Vossen AC, Galama JM, Ursem NT, Steegers EA, Wildschut HI . 2006. Incidence of parvovirus B19 infection among an unselected population of pregnant women in the Netherlands: A prospective study. Eur J Obstet Gynecol Reprod Biol 128 : 46 49.[PubMed]
129. Riipinen A, Sallmén M, Hedman L, Ojajärvi A, Lindbohm ML, Meriluoto M, Surcel HM, Taskinen H, Nuutila M, Karikoski R, Hedman K, Söderlund-Venermo M . 2014. Increased risk of human parvovirus B19 infection in day-care employees: a cohort study among pregnant workers during an epidemic in Finland. Occup Environ Med 71 : 836 841.[PubMed]
130. Koch WC, Harger JH, Barnstein B, Adler SP . 1998. Serologic and virologic evidence for frequent intrauterine transmission of human parvovirus B19 with a primary maternal infection during pregnancy. Pediatr Infect Dis J 17 : 489 494.[PubMed]
131. Public Health Laboratory Service Working Party on Fifth Disease . 1990. Prospective study of human parvovirus (B19) infection in pregnancy. BMJ 300 : 11661170.[PubMed]
132. Miller E, Fairley CK, Cohen BJ, Seng C . 1998. Immediate and long term outcome of human parvovirus B19 infection in pregnancy. Br J Obstet Gynaecol 105 : 174 178.[PubMed]
133. Chen MY, Yang SJ, Hung CC . 2011. Placental transmission of human parvovirus 4 in newborns with hydrops, Taiwan. Emerg Infect Dis 17 : 1954 1956.[PubMed]
134. Riipinen A, Väisänen E, Lahtinen A, Karikoski R, Nuutila M, Surcel HM, Taskinen H, Hedman K, Söderlund-Venermo M . 2010. Absence of human bocavirus from deceased fetuses and their mothers. J Clin Virol 47 : 186 188.[PubMed]
135. Norja P, Lassila R, Makris M . 2012. Parvovirus transmission by blood products—a cause for concern? Br J Haematol 159 : 385 393.[PubMed]
136. Drexler JF, Reber U, Muth D, Herzog P, Annan A, Ebach F, Sarpong N, Acquah S, Adlkofer J, Adu-Sarkodie Y, Panning M, Tannich E, May J, Drosten C, Eis-Hübinger AM . 2012. Human parvovirus 4 in nasal and fecal specimens from children, Ghana. Emerg Infect Dis 18 : 1650 1653.[PubMed]
137. Morey AL, Ferguson DJP, Leslie KO, Taatjes DJ, Fleming KA . 1993. Intracellular localization of parvovirus B19 nucleic acid at the ultrastructural level by in situ hybridization with digoxigenin-labelled probes. Histochem J 25 : 421 429.[PubMed]
138. Morey AL, Porter HJ, Keeling JW, Fleming KA . 1992. Non-isotopic in situ hybridisation and immunophenotyping of infected cells in the investigation of human fetal parvovirus infection. J Clin Pathol 45 : 673 678.[PubMed]
139. Anderson LJ, Török TJ, Zaki SR, . 1998. Human parvovirus B19, p 3.0 3.20. In Wilfert CM (ed), Pediatric Infectious Diseases. Current Medicine, Inc., and Churchill Livingstone, Philadelphia, PA.
140. von dem Borne AE, Bos MJ, Joustra-Maas N, Tromp JF, van't Veer MB, van Wijngaarden-du Bois R, Tetteroo PA . 1986. A murine monoclonal IgM antibody specific for blood group P antigen (globoside). Br J Haematol 63 : 35 46.[PubMed]
141. 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.[PubMed]
142. Hobbs JA . 2006. Detection of adeno-associated virus 2 and parvovirus B19 in the human dorsolateral prefrontal cortex. J Neurovirol 12 : 190 199.[PubMed]
143. Kobayashi S, Maruta A, Yamamoto T, Katayama N, Higuchi R, Sakano Y, Fujita H, Koharazawa H, Tomita N, Taguchi J, Kodama F, Nakamura Y, Shimizu A . 1998. Human parvovirus B19 capsid antigen in granulocytes in parvovirus-B19-induced pancytopenia after bone marrow transplantation. Acta Haematol 100 : 195 199.[PubMed]
144. Söderlund-Venermo M, Hokynar K, Nieminen J, Rautakorpi H, Hedman K . 2002. Persistence of human parvovirus B19 in human tissues. Pathol Biol (Paris) 50 : 307 316.[PubMed]
145. Takahashi M, Ito M, Sakamoto F, Shimizu N, Furukawa T, Takahashi M, Matsunaga Y . 1995. Human parvovirus B19 infection: immunohistochemical and electron microscopic studies of skin lesions. J Cutan Pathol 22 : 168 172.[PubMed]
146. Porter HJ, Khong TY, Evans MF, Chan VT-W, Fleming KA . 1988. Parvovirus as a cause of hydrops fetalis: detection by in situ DNA hybridisation. J Clin Pathol 41 : 381 383.[PubMed]
147. Anderson LJ . 1987. Role of parvovirus B19 in human disease. Pediatr Infect Dis J 6 : 711 718.[PubMed]
148. Kurtzman GJ, Cohen B, Meyers P, Amunullah A, Young NS . 1988. Persistent B19 parvovirus infection as a cause of severe chronic anaemia in children with acute lymphocytic leukaemia. Lancet 2 : 1159 1162.[PubMed]