Human parvovirus B19: General considerations and impact on patients with sickle-cell disease and thalassemia and on blood transfusions

FEMS Immunology and Medical Microbiology

Volumn 62, Issue 3, 2011, Pages 247-262

  Slavov, Svetoslav N ^a   Kashima, Simone ^a   Pinto, Ana Cristina Silva ^a   Covas, Dimas Tadeu ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Blood transfusion; Clinical conditions; Parvovirus B19; Sickle cell disease

Indexed keywords

HEMOGLOBIN;

BLOOD DONOR; BLOOD TRANSFUSION; BONE MARROW SUPPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN PARVOVIRUS B19; NONHUMAN; PARVOVIRUS INFECTION; PRIORITY JOURNAL; SHORT SURVEY; SICKLE CELL ANEMIA; THALASSEMIA; VIRUS DIAGNOSIS; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANEMIA, SICKLE CELL; BLOOD DONORS; BLOOD TRANSFUSION; HUMANS; PARVOVIRIDAE INFECTIONS; PARVOVIRUS B19, HUMAN; THALASSEMIA;

EID: 79960346731     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2011.00819.x     Document Type: Short Survey

References (157)

1. Amaku M, Azevedo R, Morgado de Castro R, Massad E & Coutihno F (2009) Relationship among epidemiological parameters of six childhood infections in a non-immunized Brazilian community. Mem I Oswaldo Cruz 104: 897-900.
2. Anderson A, Higgins PG, Davis LR, William JS, Jones SE, Kidd IM, Pattison JR & Tyrrell DA (1985) Experimental parvoviral infection in humans. J Infect Dis 152: 257-265.
3. Anderson M, Jones S, Fisher-Hoch S, Lewis E, Hall S, Bartlett C, Cohen B, Mortimer P & Pereira M (1983) Human parvovirus, the cause of erythema infectiosum (fifth disease)? Lancet i: 1378.
4. Assanassen C, Quinton RA & Buchanan GR (2003) Acute myocardial infarction in sickle-cell anemia. J Pediat Hematol Onc 25: 978-981.
5. Azzi A, Ciappi S, Zakarewska K, Morfini M, Mariani G & Mannucci PM (1992) Human parvovirus B19 infection in hemophiliacs first infused with two high purity, virally attenuated factor VIII concentrates. Am J Hematol 39: 228-230.
6. Azzi A, Morfini M & Mannucci PM (1999) The transfusion-associated transmission of parvovirus B19. Transfus Med Rev 13: 194-204.
7. Bakhshi S, Sarnaik S, Becker C, Shurney W, Nigro M & Savasan S (2002) Acute encephalopathy with parvovirus B19 infection in sickle cell disease. Arch Dis Child 87: 541-542.
8. Baylis S, Chudy M, Blumel J, Pisani G, Candotti D, José M & Heath A (2010) Collaborative study to establish a replacement World Health Organization International Standard for Parvovirus B19 DNA nucleic acid amplification technology (NAT)-based assays. Vox Sang 98: 441-446.
9. Bekhit M, Greenwood P, Warren R, Aarons E & Jauniaux E (2009) In utero treatment of severe foetal anaemia due to parvovirus B19 in one foetus in a twin pregnancy - a case report and literature review. Fetal Diagn Ther 25: 153-157.
10. Biesma D & Nieuwenhuis H (1997) Life-threatening anemia caused by B19 parvovirus in a non-immunocompromised patient. Neth J Med 50: 81-84.
11. Blumel J, Schmidt I, Wilkommen H & Lower J (2002) Inactivation of Parvovirus B19 during pasteurization of human serum albumin. Transfusion 42: 1011-1018.
12. Bönsch C, Kempf C & Ros C (2008) Interaction of Parvovirus B19 with human erythrocytes alters virus structure and cell membrane integrity. J Virol 82: 11784-11791.
13. Bönsch C, Kempf C, Mueller I, Manning L, Laman N, Davis T & Ros C (2010a) Chloroquine and its derivatives exacerbate B19V associated anemia by promoting viral replication. PLoS Negl Trop Dis 4: e699.
14. Bönsch C, Zuercher C, Lieby P, Kempf C & Ros C (2010b) The globoside receptor triggers structural changes in the B19 virus capsid that facilitate virus internalization. 84: 11737-11746.
15. Broliden K (2001) Parvovirus B19 infection in pediatric solid organ and bone marrow transplantation. Pediatr Transplant 5: 320-330.
16. Broliden K, Tolfvenstam T & Norbeck O (2006) Clinical aspects of parvovirus B19 infection. J Intern Med 260: 285-304.
17. Brown CS, Salimans MM, Noteborn MHM & Welland HT (1990) Antigenic parvovirus B19 coat proteins VP1 and VP2 produced in large quantities in a baculovirus expression system. Virus Res 15: 197-211.
18. Brown K (2004) Human parvoviruses. Principles and Practice of Clinical Virology (Zuckerman A, Bantavala J, Pattison J, Griffiths P & Schoub B, eds), pp. 703-721. John Wiley & Sons, Chichester.
19. Brown K (2009) Human parvoviruses. Principles and Practice of Clinical Virology (Zuckerman AJ, Bantavala JE, Schoub BD, Griffiths PD & Mortimer P, eds), pp. 853-867. John Wiley & Sons, Chichester.
20. Brown T, Anand A, Ritchie L, Clewly J & Reid T (1984) Intrauterine parvovirus infection associated with hydrops fetalis. Lancet 2: 1033-1034.
21. Cassinotti P & Siegl G (2000) Quantitative evidence for persistence of human parvovirus B19 DNA in an immunocompetent individual. Eur J Clin Microbiol 19: 886-887.
22. Cassinotti P, Bas S, Siegl G & Vischer TL (1995) Association between human parvovirus B19 infection and arthritis. Ann Rheum Dis 54: 498-500.
23. Cassinotti P, Burtonboy G, Fopp M & Sigel G (1997) Evidence for persistence of human parvovirus B19 DNA in bone marrow. J Med Virol 53: 229-232.
24. Charache S, Scott JC & Charache P (1979) 'Acute chest syndrome' in adults with sickle cell anemia. Microbiology, treatment, and prevention. Arch Intern Med 139: 67-69.
25. Chen AY & Qiu J (2010) Parvovirus infection-induced cell death and cell cycle arrest. Future Virol 5: 731-743.
26. Chen H, Zhang J, Yang S, Ma LN, Ma YP, Liu XT, Cai XP, Zhang YG & Liu YS (2009) Rapid detection of porcine parvovirus DNA by sensitive loop-mediated isothermal amplification. J Virol Methods 158: 100-103.
27. Chiorini JA, Wiener SM, Yang L, Smith RH, Safer B, Kilcoin NP, Liu Y, Urcelay E & Kotin RM (1996) The roles of Rep proteins in gene expression and targeted integration. Curr Top Microbiol 218: 25-33.
28. Clewley J (1984) Biochemical characterization of a human parvovirus. J Gen Virol 65: 241-245.
29. Cohen BJ, Beard S, Knowles WA, Ellis JS, Joske D, Goldman JM, Hewitt P & Ward KN (1997) Chronic anemia due to parvovirus B19 infection in a bone marrow transplant patient after platelet transfusion. Transfusion 37: 947-952.
30. Corcoran A & Doyle S (2004) Advances in the biology, diagnosis and host-pathogen interactions of parvovirus B19. J Med Microbiol 53: 459-475.
31. Corcoran A, Doyle S, Waldron D, Nichholson A & Mahon BP (2000) Impaired gamma interferon responses against parvovirus B19 by recently infected children. J Virol 74: 9903-9910.
32. Corcoran A, Mahon BP & Doyle S (2004) B cell memory is directed toward conformational epitopes of parvovirus B19 capsid proteins and unique region of VP1. J Infect Dis 189: 1873-1880.
33. Corsini J, Tal J & Winocour E (1997) Directed integration of minute virus of mice DNA into episomes. J Virol 71: 9008-9015.
34. Cossart Y, Field A, Cant B & Widdows D (1975) Parvovirus-like particles in human sera. Lancet 1: 72-73.
35. Daly P, Corcoran A, Mahon PB & Doyle S (2002) High-sensitivity PCR detection of parvovirus B19 in plasma. J Clin Microbiol 40: 1958-1962.
36. Deiss V, Tratschin J, Weitz M & Siegl G (1990) Cloning of the human parvovirus B19 genome and structural analysis of its palindromic termini. Virology 175: 247-254.
37. Doyle S (2011) The detection of parvoviruses. Methods Mol Biol 665: 213-231.
38. Escher F, Kuhl U, Sabi T, Suckau L, Lassner D, Poller W, Schultheiss HP & Noutsias M (2008) Immunohistological detection of Parvovirus B19 in endomyocardial biopsies from dilated cardiomyopathy patients. Med Sci Monitor 14: CR333-CR338.
39. Fartoukh M, Prigent H, Thioliere B, Enache-Angoulvant A, Garbarg-Chenon A & Girot R (2006) Fatal fungal superinfection complicating B19-virus induced massive bone-marrow necrosis in sickle-cell disease. Haematologica 91: ECR18.
40. Fattet S, Cassinotti P & Popovic MB (2004) Persistent human parvovirus B19 infection in children under maintenance chemotherapy for acute lymphocytic leukemia. J Pediat Hematol Onc 26: 497-503.
41. Ferguson M, Walker D & Cohen B (1997) Report of a collaborative study to establish the international standard for parvovirus B19 serum IgG. Biologicals 3: 283-288.
42. Ferry T, Hirshel B, Dang T et al. (2010) Swiss HIV cohort study infrequent replication of Parvovirus B19 and erythrovirus genotype 2 and 3 among HIV infected patients with chronic anemia. Clin Infect Dis 50: 115-118.
43. Franssila R, Auramo J, Modrow S, Mobs M, Oker-Blom C, Kapyla P, Soderlund-Venermo M & Hedman K (2005) T-helper cell-mediated interferon-gamma expression after human parvovirus B19 infection: persistent VP2 specific and transient VPu-specific activity. Clin Exp Immunol 142: 53-61.
44. Freitas RB, Melo FL, Oliveira DS, Romano CM, Freitas MR, Macêdo O, Linhares AC, de A Zanotto PM & Durigon EL (2008) Molecular characterization of human erythrovirus B19 strains obtained from patients with several clinical presentations in the Amazon region of Brazil. J Clin Virol 43: 60-65.
45. Geng Y, Wu CG, Bhattacharyya SP, Tan D, Guo ZP & Yu MW (2007) Parvovirus B19 DNA in factor VIII concentrates: effects of manufacturing procedures and B19 screening by nucleic acid testing. Transfusion 47: 883-889.
46. Godeau B, Galacteros F, Schaeffer A, Morinet F, Bachir D, Rosa J & Portos JL (1991) Aplastic crisis due to extensive bone-marrow necrosis and human parvovirus infection in sickle cell disease. Am J Med 91: 557-558.
47. Grabarczyk P, Kalinska A, Kara M, Wieczorek R, Ejduk A, Sulkowska E, Gołebiowska-Staroszczyk S, Matysiak M, Baylis S & Brojer E (2011) Identification and characterization of acute infection with parvovirus B19 genotype 2 in immunocompromised patients in Poland. J Med Virol 83: 142-149.
48. Gray J, Cohen B & Desselberger U (1993) Detection of human parvovirus B-19- specific IgM and IgG antibodies using a recombinant viral VP1 antigen expressed in insect cells and estimation of time of infection by testing antibody avidity. J Virol Methods 44: 11-23.
49. Guan W, Cheng F, Yoko Y, Kleiboeker S, Wong S, Zhi S, Pintel DJ & Qiu J (2008) Block to the production of full length B19 virus transcripts by internal polyadenylation is overcome by replication of the viral genome. J Virol 82: 9951-9963.
50. Guillaume MP, Hermanus M & Peretz A (2002) Unusual localization of chronic arthropathy in lumbar facet joints after parvovirus B19 infection. Clin Rheumatol 21: 306-308.
51. Gupta R & Singh T (2005) Parvovirus B19 co-infection with falciparum malaria: a cause of severe anemia. Haematologica 90: ECR41.
52. Gustafsson I, Kaldensjo T, Lindblom A, Norbeck O, Henter J, Tolfvenstam T & Broliden K (2010) Evaluation of Parvovirus B19 infection in children with malignant or hematological disorders. Clin Infect Dis 50: 1426-1427.
53. Heegaard E & Brown K (2002) Human Parvovirus B19. Clin Microbiol Rev 15: 485-505.
54. Heegard E, Qvortrup K & Christensen J (2002) Baculovirus expression of erythrovirus V9 capsids and screening by ELISA: serologic cross-reactivity with erythrovirus B19. J Med Virol 66: 246-252.
55. Hemauer A, von Poblotzki A, Gigler A, Cassinotti P, Siegl G, Wolf H & Modrow S (1996) Sequence variability among different parvovirus B19 isolates. J Gen Virol 77: 1781-1785.
56. Hourfar M, Mayr-Wohlfart U, Themann A, Sireis W, Seifried E, Schrezenmeier H & Schmidt M (2011) Recipients potentially infected with Parvovirus B19 by red cell blood products. Transfusion 5: 129-136.
57. Hsu S, Chen Y, Huang Y, Yeh TT, Chen WC, Ho ES & Chou MM (2007) Prenatal diagnosis and perinatal management of maternal-fetal congenital parvovirus B19 infection. Taiwan J Obstet Gynecol 46: 417-422.
58. Ingrassia F, Gadaleta A, Maggi P & Pastore G (2010) Plasmodium falciparum malaria and Parvovirus B19; a case of acute co-infection. BMC Infect Dis 10: 87.
59. International Committee on Taxonomy of Viruses (ICTV) (2007) Virus taxonomy: 2007 release. Virology division, IUMS. Available at.
60. Iwa N & Yutani C (1995) Cytodiagnosis of Parvovirus B19 infection from ascites fluid of hydrops fetals: report of a case. Diagn Cythopathol 13: 139-141.
61. Jitschin R, Peters O, Plentz A, Turiwski P, Segerer H & Modrow S (2010) Impact of parvovirus B19 infection on paediatric patients with hematological and/or oncological disorders. Clin Microbiol Infec DOI: DOI: 10.1111/j.1469-0691.2010.03355.x.
62. Jones MS, Kapoor A, Lukashov VV, Simmonds P, Hecht F & Delwart E (2005) New DNA viruses identified in patients with acute infection syndrome. J Virol 79: 8230-8236.
63. Jones PH, Pickett LC, Anderson MJ & Pasvol G (1990) Human parvovirus infection in children and severe anaemia seen in an area endemic for malaria. J Trop Med Hyg 93: 67-70.
64. Jordan J, Tiangco B, Kiss J & Koch W (1998) Human Parvovirus B19: prevalence of viral DNA in volunteer blood donors and clinical outcomes in transfusion recipients. Vox Sang 75: 97-102.
65. Kaufman B, Simpson A & Rossmann M (2004) The structure of human parvovirus B19. P Natl Acad Sci USA 101: 11628-11633.
66. Ke L, He M, Li C et al. (2011) The prevalence of human parvovirus B19 DNA and antibodies in blood donors from four Chinese blood centers. Transfusion DOI: DOI: 10.1111/j.1537-2995.2011.03067.x.
67. Kelly H, Siebert D, Hammond R, Leydon J, Kiley P & Maskill W (2000) The age-specific prevalence of human parvovirus immunity in Victoria, Australia compared to other parts of the world. Epidemiol Infect 124: 449-457.
68. Kerr JR, Curran MD, Moore JE, Coyle PV & Ferguson WP (1995) Persistent parvovirus infection. Lancet 345: 1118.
69. Kerr S, O'Keeffe G, Kilty C & Doyle S (1999) Undenatured parvovirus B19 antigens are essential for the accurate detection of parvovirus B19 IgG. J Med Virol 57: 179-185.
70. Kinney JS, Anderson LJ, Farrar J, Strikas RA, Kumar ML, Kliegman RM, Sever JL, Hurwitz ES & Sikes RK (1988) Risk of adverse outcomes of pregnancy after human parvovirus B19 infection. J Infect Dis 157: 663-667.
71. Klein HG (1999) Immunomodulatory aspects of transfusion. A once and future risk? Anesthesiology 91: 861-865.
72. Koduri P & Naides S (1996) Transient blood plasmacytosis in Parvovirus B19 infection: a report of two cases. Ann Hematol 72: 49-51.
73. Kooistra K, Mesman H, de Waal M, Koppelman M & Zaaijer H (2011) Epidemiology of high-level parvovirus B19 viraemia among Dutch blood donors, 2003-2009. Vox Sang 100: 261-266.
74. Koppelman MH, van Swieten P & Cuijpers HT (2010) Real-time polymerase chain reaction of parvovirus B19 DNA in blood donations using a commercial and in-house assay. Transfusion DOI: DOI: 10.1111/j.1537-2995.2010.02995.x.
75. Krishnamurti L, Lanford L & Munoz R (2007) Life-threatening parvovirus B19 and herpes simplex virus associated acute myocardial dysfunction in a child with sickle cell disease. Pediatr Blood Cancer 49: 1019-1021.
76. Kudesia G & Wreighitt T (2005) Parvovirus B19. Clinical and Diagnostic Virology (Kudesia G & Wreighitt T, eds), pp. 90-93. Cambridge University Press, Cambridge.
77. Kurtzman GJ, Cohen BJ, Field AM, Oseas R, Blaese RM & Young NS (1989) Immune response to B19 parvovirus and an antibody defect in persistent viral infection. J Clin Invest 84: 1114-1123.
78. Lamont R, Sobel J, Vaisbuch E, Kusanovic J, Mazaki-Tovi S, Kim S, Uldbjerg N & Romero R (2010) Parvovirus B19 infection in human pregnancy. B J Obste Gynaecol 118: 175-186.
79. Landolsi H, Yacoubi MT, Bouslama L, Lahmar A, Trabelsi A, Hmissa S, Aouni M & Korbi S (2009) Detection of the human parvovirus B19 in nonimmune hydrops fetalis using immunohistochemistry and nested-PCR in formalin fixed and paraffin embedded placenta and fetal tissues. Pathol Biol 57: e1-e7.
80. Lefrere J, Servant-Delmas A, Candotti D, Mariotti M, Thomas I, Brossard Y, Lefrere F, Girot R, Allain JP & Laperche S (2005) Persistent B19 infection in immunocompetent individuals: implications for transfusion safety. Blood 106: 2890-2895.
81. Lefrere JJ & Bourgeois H (1986) Human parvovirus associated with erythroblastopenia in iron deficiency anemia. J Clin Pathol 39: 1277-1278.
82. Lefrere JJ, Courouce AM, Bertrand Y, Girot R & Soulier JP (1986a) Human parvovirus and aplastic crisis in chronic hemolytic anemias: a study of 24 observations. Am J Hematol 23: 271-275.
83. Lefrere JJ, Courouce AM, Girot R & Cornu P (1986b) Human parvovirus and thalassemia. J Infection 13: 45-49.
84. Lowenthal E, Wells A, Emanuel P, Player R & Prchal JT (1996) Sickle cell acute chest syndrome associated with Parvovirus B19 infection. Am J Hematol 51: 207-213.
85. Lunardi C, Tinazzi E, Bason C, Dolcino M, Corrocher R & Puccetti A (2008) Human parvovirus B19 infection and autoimmunity. Autoimmun Rev 8: 116-120.
86. Lyon DJ, Chapman CS, Martin C, Brown KE, Clewley JP, Flower AJ & Mitchell VE (1989) Symptomatic parvovirus B19 infection and heat-treated factor IX concentrate. Lancet i: 1085.
87. Manaresi E, Zuffi E, Gallinella G, Gentilomi G, Zebrini M & Musiani M (2001) Differential IgM response to conformational and linear epitopes of parvovirus B19 VP1 and VP2 structural proteins. J Med Virol 64: 67-73.
88. Michel P, Makela A, Korhonen E, Toivola J, Hedman L, Söderlund-Venermo M, Hedman K & Oker-Blom C (2008) Purification and analysis of polyhistidine-tagged human parvovirus B19 VP1 and VP2 expressed in insect cells. J Virol Methods 152: 1-5.
89. Modrow S, Wenzel J, Schimanski S, Schwarzbeck J, Rothe U, Oldenburg J, Jilg W & Eis-Hubinger A (2010) Prevalence of nucleic acid sequences specific for human parvoviruses, hepatitis A and hepatitis E viruses in coagulation factor concentrates. Vox Sang 100: 351-358.
90. Moffat S, Yaegashi N & Tada K (1998) Human parvovirus nonstructural protein (NS1) induces apoptosis in erythroid lineage cells. J Virol 74: 3018-3028.
91. Mori J, Beattie P, Melton DW, Cohen B & Clewly J (1987) Structure and mapping of the DNA of human parvovirus B19. J Gen Virol 68: 2797-2806.
92. Morita E, Tada K, Chisaka H, Asao H, Sato H, Yaegashi N & Sugamura K (2001) Human parvovirus B19 induces cell cycle arrest at G2 phase with accumulation of mitotic cyclins. J Virol 75: 7555-7563.
93. Munro K, Croxson MC, Thomas S & Wilson NJ (2003) Three cases of myocarditis in childhood associated with human parvovirus (B19 virus). Pediatr Cardiol 24: 473-475.
94. Newton C, Warn P, Winstanley P, Peshu N, Snow R, Pasvol G & Marsh K (1997) Severe anaemia in children living in a malaria endemic area of Kenya. Trop Med Int Health 2: 165-178.
95. Norja P, Hokynar K, Aaltonen LM et al. (2006) Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. P Natl Acad Sci USA 103: 7450-7453.
96. Ozawa K, Kurtzman G & Young N (1986) Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233: 883-886.
97. Ozawa K, Ayub J, Yu-Shu H, Kurtzman G, Shimada T & Young N (1987) Novel transcription map of the B19 (human) pathogenic parvovirus. J Virol 61: 2395-2406.
98. Pallier C, Greco A, Le Junter J, Saib A, Vassais I & Morinet F (1997) The 3' untranslated region of B19 parvovirus capsid protein mRNAs inhibits its own mRNA translation in nonpermissive cells. J Virol 71: 9482-9489.
99. Pankuweit S, Ruppert R, Eckhardt H, Strache D & Maisch B (2005) Pathophysiology and aetiological diagnosis of inflammatory myocardial diseases with a special focus on Parvovirus B19. J Vet Med B 52: 344-347.
100. Parsyan A, Szmaragd C, Allain JP & Candotti D (2007) Identification and genetic diversity of two human parvovirus genotype 3 subtypes. J Gen Virol 88: 428-431.
101. Pasquinelli G, Bonvicini F, Foroni L, Salfi N & Galinella G (2009) Placental endothelial cells can be productively infected by Parvovirus B19. J Clin Virol 44: 33-38.
102. Pasvol G (2006) Parvovirus infection, malaria and anemia in the tropics - a new hidden enemy. J Infect Dis 194: 141-142.
103. Pattison J, Jones S, Hodgson J, Davis L, White J, Stroud C & Murtaza L (1981) Parvovirus infections and hypoplastic crisis in sickle-cell anemia. Lancet i: 664-665.
104. Prowse C, Ludlam C & Yap P (1997) Human Parvovirus B19 and blood transfusions. Vox Sang 72: 1-10.
105. Quek L, Sharpe C, Dutt N, Height S, Allman M, Awogbade M, Rees D, Zuckerman M & Thein S (2010) Acute human parvovirus B19 infection and nephrotic syndrome in patients with sickle-cell disease. Brit J Haematol 149: 289-291.
106. Rayburg M, Kalinyak K, Towbin A, Baker P & Joiner C (2010) Fatal bone marrow embolism in child with hemoglobin SE disease. Am J Hematol 85: 182-184.
107. Reed JL, Kucukcetin B & Koering S (2000) Mechanisms of parvovirus B19 persistence in peripheral blood mononuclear cells (PBMC). Infect Dis Rev 2: 169.
108. Reid D, Reid T, Brown T, Rennie J & Eastmond C (1985) Human parvovirus-associated arthritis: a clinical and laboratory description. Lancet i: 422-425.
109. Reitblat T, Drogenikov T, Sigalov I, Oren S & London D (2000) Transient anticardiolipin antibody syndrome in a patient with parvovirus B19 infection. Am J Med 109: 512-513.
110. Ros C, Baltzer C, Mani B & Kempf C (2006) Parvovirus uncoating in vitro reveals a mechanism of DNA release without capsid disassembly and striking differences in encapsidated DNA stability. Virology 345: 137-147.
111. Saarinen UM, Chorba TL, Tattersall P, Young NS, Anderson LJ, Palmer E & Coccia PF (1986) Human parvovirus B19-induced epidemic red cell aplasia in patients with hereditary hemolytic anemia. Blood 67: 1411-1417.
112. Saldanha J (2001) Validation and standardization of nucleic acid amplification technology (NAT) assay for the detection of viral contamination of blood and blood products. J Clin Virol 20: 7-13.
113. Saldanha J, Lelie N, Yu MW & Heath A (2002) Collaborative study group. Establishment of the first World Health Organization International Standard for human Parvovirus B19 nucleic acid amplification techniques. Vox Sang 82: 24-31.
114. Salimans M, Holsappel S, van de Rijke F, Jiwa NM, Raap AK & Weiland HT (1989) Rapid detection of human parvovirus B19 DNA by dot-hybridization and the polymerase chain reaction. J Virol Methods 23: 19-28.
115. Sanphasitvong W, Poovorawan K, Boonsuk P, Assanasen T, Na Nakorn T & Poovorawan Y (2005) Parvovirus B19 infection in HIV patient with pure red cell aplasia. Southeast Asian J Trop Med Public Health 36: 1216-1220.
116. 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°C heat after lyophilization. Transfusion 37: 517-522.
117. Satake M, Hoshi Y, Taira R, Momose S, Hino S & Tadokoro K (2011) Symptomatic parvovirus B19 infection caused by blood component transfusion. Transfusion DOI: DOI: 10.1111/j.1537-2995.2010.03047.x.
118. Scarlata F, Gianelli E, Miceli S, Galimberti L & Antinori S (2002) Acute Parvovirus infection and anemia during Plasmodium falciparum malaria. Clin Infect Dis 35: 1449-1450.
119. Serjeant GR, Topley JM, Mason K, Serjeant BE, Pattison JR, Jones SE & Mohamed R (1981) Outbreak of aplastic crises in sickle cell anemia associated with parvovirus-like agent. Lancet 2: 595-597.
120. Servant À, Laperche S, Lallemand F, Marinho V, De Saint Maur G, Meritet J & Garbag-Chenon A (2002) Genetic diversity within human erythroviruses: identification of three genotypes. J Virol 76: 9124-9134.
121. Servey J, Reamy B & Hodge J (2007) Clinical presentations of parvovirus B19 infection. Am Fam Physician 75: 373-376.
122. Shackelton LA & Holmes EC (2006) Phylogenetic evidence for rapid evolution of human parvovirus B19. J Virol 80: 3666-3669.
123. Simeoni S, Puccetti A, Tinazzi E & Lunardi C (2010) Parvovirus B19. Molecular Detection of Human Viral Pathogens (Liu D, ed), pp. 831-834. CRC Press, Taylor and Francis Group, Boca Raton, FL.
124. Simmonds P, Douglas J, Bestetti G, Longhi E, Antinori S, Paravicini C & Corbellino M (2008) A third genotype of the human parvovirus PARV4 in sub-Saharan Africa. J Gen Virol 89: 2299-2302.
125. Smith-Whitley K, Zhao H, Hodinka R, Kwiatkowski J, Cecil R, Cecil T, Cnaan A & Ohene-Frempong K (2003) Epidemiology of human parvovirus B19 in children with sickle-cell disease. Blood 103: 422-427.
126. Sol N, Junter J, Vassias I, Freyssiner J, Thomas A, Prigent A, Rudkin B, Fichelson S & Morinet F (1999) Possible interactions between the NS-1 protein and tumor necrosis factor-alpha pathways in erythroid cell apoptosis induced by human parvovirus B19. J Virol 73: 8762-8770.
127. Soliman Oel-S, Abd El-Aal M, El-Ashry L, Zaghloul M & Kora B (2009) Parvovirus B19 infection in pediatric oncology patients: diagnostic value of clinical and serologic parameters compared with nested PCR. J Pediat Hematol Onc 31: 173-176.
128. St Amand J, Beard C, Humphries K & Astell C (1991) Analysis of splice junctions and in vitro and in vivo translation potential of the small, abundant B19 parvovirus RNAs. Virology 183: 133-142.
129. Stramer SL, Hollinger FB, Katz LM, Kleinman S, Metzel PS, Gregory KR & Dodd RY (2009) Emerging infectious disease agents and their potential threat to transfusion safety. Transfusion 49: 1S-29S.
130. Summers J, Jones S & Anderson M (1983) Characterization of the genome of the agent of erythrocyte aplasia permits its classification as a human parvovirus. J Gen Virol 64: 2527-2532.
131. Toan NL, Duechting A, Kremsner PG et al. (2006) Phylogenetic analysis of human parvovirus B19, indicating two subgroups of genotype 1 in Vietnamese patients. J Gen Virol 87: 2941-2949.
132. Tolaymat A, Al Mousily F, MacWilliam K, Lammert N & Freeman B (1999) Parvovirus glomerulonephritis in a patient with sickle cell disease. Pediatr Nephrol 13: 340-342.
133. Tolfvenstam T & Broliden K (2009) Parvovirus B19 infection. Semin Fetal Neonat M 14: 218-221.
134. Toyokawa Y, Kingetsu I, Yasuda C, Yasuda J, Yoshida K, Kurosaka D & Yamada A (2007) A case of pure red cell aplasia complicated by Evans syndrome. Mod Rheumatol 17: 333-337.
135. US Food and Drug Administration (2008) Nucleic Acid Testing (NAT) to Reduce the Possible Risk of Parvovirus B19 Transmission by Plasma-Derived Products. FDA Center for Biologics Evaluation and Research, FDA Draft Guidance for Industry, Rockville, MD.
136. Van Elsacker-Niele AM, Salimans MM, Weiland HT, Vermey-Keers C, Anderson MJ & Versteeg J (1989) Fetal pathology in human parvovirus B19 infection. Br J Obstet Gynaecol 96: 768-775.
137. Von Landenberg P, Lehmann HW, Knoll A, Dorsch S & Modrow S (2003) Antiphospholipid antibodies in pediatric and adult patients with rheumatic disease are associated with parvovirus B19 infection. Arthritis Rheum 48: 1939-1947.
138. Wan C, Soderlund-Venermo M, Pintel D & Riley K (2002) Molecular characterization of three newly recognized rat parvoviruses. J Gen Virol 83: 2075-2083.
139. Watanabe D, Taniguchi T, Otani N, Tominari S, Nishida Y, Uehira T & Shirasaka T (2010) Immune reconstitution to parvovirus B19 and resolution of anemia in a patient treated with highly active retroviral therapy. J Infect Chemother 17: 283-287.
140. Weigel-Kelley K, Yoder M & Srivastava A (2003) Alpha-5 beta-1 integrin as a cellular co-receptor for human parvovirus B19: requirement of functional activation of beta1 integrin for viral entry. Blood 102: 3927-3933.
141. Weigel-Kelley KA, Yoder MC, Chen L & Srivastava A (2006) Role of integrin cross-regulation in parvovirus B19 targeting. Hum Gene Ther 17: 909-920.
142. Weiland HL, Salimans MM, Fibbew NE, Kluin PM & Cohen BJ (1989) Prolonged parvovirus B19 infection with severe anemia in a bone marrow transplant patient. Br J Haematol 71: 300.
143. White D & Fenner F (1994) Parvoviridae. Medical Virology, 4th edn (White D & Fenner F, eds), pp. 285-293. Academic Press, San Diego.
144. White D, Woolf A, Mortimer P, Cohen B, Blake D & Bacon P (1985) Human parvovirus arthropathy. Lancet i: 419-421.
145. Wierenga K, Pattison J, Brink N, Griffiths M, Miller M, Shah DJ, Williams W, Serjeant BE & Serjeant GR (1995) Glomerulonephritis after human parvovirus infection in homozygous sickle-cell disease. Lancet 346: 475-476.
146. Wierenga KJ, Serjeant BE & Serjeant GR (2001) Cerebrovascular complications and parvovirus infection in homozygous sickle cell disease. J Pediatr 13: 438-442.
147. 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.
148. 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.
149. Yaegashi N, Niinuma T, Chisaka H, Watanabe T, Uehara S, Okamura K, Moffat S, Sugamura K & Yajima A (1998) The incidence of, and factors leading to, parvovirus B19-related hydrops fetalis following maternal infection; report of 10 cases and meta-analysis. J Infection 37: 28-35.
150. Yates A, Hankins J, Mortier N, Aygun B & Ware R (2009) Simultaneous acute splenic sequestration and transient aplastic crisis in children with sickle cell disease. Pediatr Blood Cancer 53: 479-481.
151. Yeats J, Daley H & Hardie D (1999) Parvovirus B19 infection does not contribute significantly to severe anaemia in children with malaria in Malawi. Eur J Haematol 63: 276-277.
152. Yu M, Alter HJ, Virata-Theimer MLA, Geng Y, Ma L, Schechterly C, Colvin C & Luban N (2010) Parvovirus B19 infection transmitted by transfusion of red blood cells confirmed by molecular analysis of linked donor and recipient samples. Transfusion 50: 1712-1721.
153. Yunoki M, Urayama T, Tsujikawa M, Sasaki Y, Abe S, Takechi K & Ikuta K (2004) Inactivation of B19 by liquid heating incorporated in the manufacturing process of human intravenous immunoglobulin preparations. Br J Haematol 128: 401-404.
154. Zaki M & Ashray R (2010) Clinical and hematological study for Parvovirus B19 infection in children with acute leukemia. Int J Lab Hematol 32: 159-166.
155. Zaki M, Hassan S, Seleim T & Lateef R (2006) Parvovirus B19 infection in a children with a variety of hematological disorders. Hematology 11: 261-266.
156. Zanella A, Rossi F, Cesana C, Foresti A, Nador F, Binda A, Lunghi G, Cappellini M, Furione M & Sirchia G (1995) Transfusion-transmitted human parvovirus B19 infection in a thalassemic patient. Transfusion 35: 769-772.
157. Zhi N, Mills I, Lu J, Wong S, Filippone C & Brown K (2006) Molecular and functional analyses of a human parvovirus B19 infectious clone demonstrates essential roles for NS1, VP1, and the 11-kilodalton protein in virus replication and infectivity. J Virol 80: 5941-5950.