Parvovirus-B 19-Infektion in der Schwangerschaft

Zusammenfassung

Das humanpathogene Parvovirus B 19 gehört zur Familie der Parvoviridae und weist einen ausgeprägten Tropismus für die erythropoiden Vorläuferzellen auf. Bei Kindern verursacht das Virus das Erythema infectiosum (Ringelröteln). Inzwischen wird die Parvovirus-B 19-Infektion mit einem weiten Spektrum von hämatologischen und nichthämatologischen Komplikationen in Zusammenhang gebracht (z. B. Leberversagen, Hepatitis, aplastische Krisen vor allem mit chronischen hämolytischen Anämien, chronische Arthritis, Arthralgien / Arthritis, transiente / persistierende Anämien, Vaskulitis, Glomerulonephritiden). Intrauterine Infektionen können bei Überleben des Fetus zu spezifischen oder permanenten Organdefekten führen (z. B. Herzanomalien, Augenerkrankungen, Lippen-Kiefer-Gaumenspalte, Mikrognathie, chronische Anämie, Myokarditis, Hepatitis, Mekoniumperitonitis und ZNS-Anomalien). Parvovirus B 19 konnte mit einem Hydrops fetalis und intrauterinem Fruchttod bei Infektionen in der Schwangerschaft assoziiert werden. Ein sicherer Zusammenhang zwischen Missbildung und B 19-Infektion ist noch nicht gewährleistet. Zum weiteren Ausschluss von teratogenen Effekten und fetalen Schäden sollte der Ausgang von B 19-infizierten Schwangerschaften überwacht und kontrolliert werden. Obwohl kongenitale Malformationen nach Parvovirusinfektion berichtet worden sind, scheint dies allerdings ein seltenes Phänomen zu sein. Eine intrauterine Therapie mit Erythrozytenkonzentrat könnte bei Hydrops fetalis und erniedrigten Hämoglobinwerten durchgeführt werden. Untersuchungen zur Entwicklung und klinischen Testung eines effizienten Impfstoffes gegen Parvovirus B 19 sind zzt. in Vorbereitung.

Abstract

The parvovirus B 19 is part of the family of the parvoviridae and shows a distinctive tropism for erythropoid precursor cells. The virus causes in children the erythema infectiosum (German measles). Meanwhile, parvovirus B 19 infections can be associated with a wide spectrum of hematological and non-hematological complications (e. g. liver failure, hepatitis, aplastic crises primarily in association with chronic hemolytic anaemias, chronic arthritis, arthralgia / arthritis, transient / persistent anaemias, vaskulitis, glomerulonephritis). Intrauterine infections can lead to specific or permanent organ defects (e. g. heart anomalies, eye diseases, micrognathy, chronic anaemia, myocarditis, hepatitis, mekonium peritonitis and central nervous system anomalies). Parvovirus B 19 infections are also associated with hydrops fetalis and intrauterine death during pregnancy. A definite relation between fetal malformations and B 19 infection has not been accomplished yet. Pregnancies complicated by parvovirus B 19 infection should be followed for further exclusion of any teratogenic effect. Although congenital malformations after a parvovirus infection are possible, this phenomenon seems to be rare. An intrauterine therapy with packed red cells could be performed for hydrops fetalis and low haemoglobin concentration. Investigation for the development and clinical testing of an efficient vaccine against parvovirus B 19 is currently in progress.

Schlüsselwörter

Parvovirus - fetale Schädigung - kongenitale Anomalien - Diagnose - Therapie

Key words

parvovirus - fetal malformation - congenital anomalies - diagnosis - therapy

Literatur

• 1 Cossart Y E, Field A M, Cant B, Widdows D. Parvovirus like particles in human sera.  Lancet. 1975;  1 72-73
• 2 Anderson M J, Lewis E, Kidd I M, Hall S M, Cohen B J. An outbreak of erythema infectiosum associated with human parvovirus infection.  J Hyg (Lond). 1984;  93 85-93
• 3 Jordan E K, Sever J L. Fetal damage caused by parvoviral infections.  Reprod Toxicol. 1994;  8 161-189
• 4 Brown T, Anand A, Richie L D, Clewly I P, Reid T MS. Intrauterine parvovirus infection associated with hydrops fetalis.  Lancet. 1984;  2 (8410) 1033-1034
• 5 Cohen B. Parvovirus B 19: an expanding spectrum of disease.  Bmj. 1995;  311 1549-1552
• 6 Kinney J S, Anderson L J, Farrar J, Strikas R A, Kumar M L, Kliegman R M, Sever J L, Hurwitz E S, Sikes R K. Risk of adverse outcomes of pregnancy after human parvovirus B 19 infection.  J Infect Dis. 1988;  157 663-667
• 7 Heegaard E D, Peterslund N A, Hornsleth A. Parvovirus B 19 infection associated with encephalitis in a patient suffering from malignant lymphoma.  Scand J Infect Dis. 1995;  27 631-633
• 8 Mylonas I, Friese K. Infektionsbedingte fetale Schädigungen. In: Ganten D, Ruckpaul W (eds). Grundlagen der Molekularmedizin - Fetale und Neonatale Schädigungen. Springer, Berlin, Heidelberg, New York, Tokio 2004
• 9 Mitchell L A. Parvovirus B 19 non-structural (NS 1) protein as a transactivator of Interleukin-6 synthesis: commom pathway in inflammatory sequelae of human parvovirus infections?.  J Med Virol. 2002;  67 267-274
• 10 Brown K E, Anderson S M, Young N S. Erythrocyte p antigen: cellular receptor for B 19 parvovirus.  Science. 1993;  262 114-117
• 11 Jordan J A, DeLoia J A. Globoside expression within the human placenta.  Placenta. 1999;  20 103-108
• 12 Marcus D M, Kundu S K, Suzuki A. The P blood group systern: Recent progress in immunochemistry and genetics.  Semin Hematol. 1981;  18 63-71
• 13 Brown K E, Hibbs J R, Gallinella G, Anderson S M, Lehman E D, McCarthy P, Young N S. Resistance to parvovirus B 19 infection due to lack of virus receptor (erythrocyte P antigen).  N Engl J Med. 1994;  330 1192-1196
• 14 Hong A R, Croitoru D P, Nguyen L T, Laberge J M, Homsy Y, Kiruluta G H. Congenital urethral fistula with normal anus: a report of two cases.  J Pediatr Surg. 1992;  27 1278-1280
• 15 McOmish F, Yap P L, Jordan A, Hart H, Cohen B J, Simmonds P. Detection of parvovirus B 19 in donated blood: a model system for screening by polymerase chain reaction.  J Clin Microbiol. 1993;  31 323-328
• 16 Enders G. Röteln und Ringelröteln. In: Friese K, Kachel W (eds). Infektionserkrankungen der Schwangeren und des Neugeborenen, 2. Aufl. Springer, Berlin, Heidelberg, New York, Tokio 1998; 67-79
• 17 Gay N J, Hesketh L M, Cohen B J, Rush M, Bates C, Morgan-Capner P, Miller E. Age specific antibody prevalence to parvovirus B 19: how many women are infected in pregnancy?.  Commun Dis Rep CDR Rev. 1994;  4 R 104-R 107
• 18 Anand A, Gray E S, Brown T, Clewley J P, Cohen B J. Human parvovirus infection in pregnancy and hydrops fetalis.  N Engl J Med. 1987;  316 183-186
• 19 Eis-Hubinger A M, Dieck D, Schild R, Hansmann M, Schneweis K E. Parvovirus B 19 infection in pregnancy.  Intervirology. 1998;  41 178-184
• 20 Prospective study of human parvovirus (B 19) infection in pregnancy. Public Health Laboratory Service Working Party on Fifth Disease.  Bmj. 1990;  300 1166-1170
• 21 Yaegashi N, Niinuma T, Chisaka H, Watanabe T, Uehara S, Okamura K, Moffatt S, Sugamura K, Yajima A. The incidence of, and factors leading to, parvovirus B 19-related hydrops fetalis following maternal infection; report of 10 cases and meta-analysis.  J Infect. 1998;  37 28-35
• 22 Enders M, Weidner A, Zoellner I, Searle K, Enders G. Fetal morbidity and mortality after acute human parvovirus B 19 infection in pregnancy: prospective evaluation of 1 018 cases.  Prenat Diagn. 2004;  24 513-518
• 23 Rodis J F, Borgida A F, Wilson M, Egan J F, Leo M V, Odibo A O, Campbell W A. Management of parvovirus infection in pregnancy and outcomes of hydrops: a survey of members of the Society of Perinatal Obstetricians.  Am J Obstet Gynecol. 1998;  179 985-988
• 24 Gilbert G L. Parvovirus B 19 infection and its significance in pregnancy.  Commun Dis Intell. 2000;  24 69-71
• 25 Kurtzmann G J, Cohen B, Field A M, Oseas R, Blaese R M, Young N S. Immune response to B 19 parvovirus and an antibody defect in persistent viral infection.  J Clin Invest. 1989;  84 1114-1123
• 26 Poblotzki A, Gerdes C, Reischl U, Wolf H, Modrow S. Lymphoproliferative responses after infection with human parvovirus B 19.  J Virol. 1996;  70 7327-7330
• 27 Moore T L. Parvovirus-associated arthritis.  Curr Opin Rheumatol. 2000;  12 289-294
• 28 Takahashi Y, Murai C, Ishii T, Sugamura K, Sasaki T. Human parvovirus B 19 in rheumatoid arthritis.  Int Rev Immunol. 1998;  17 309-321
• 29 Reid D M, Reid T M, Brown T, Rennie J A, Eastmond C J. Human parvovirus-associated arthritis: a clinical and laboratory description.  Lancet. 1985;  1 422-425
• 30 Jobanputra P, Davidson F, Graham S, O'Neill S, Simmonds P, Yap P L. High frequency of parvovirus B 19 in serum samples submitted for a rheumatoid factor test.  Br Med J. 1995;  311 1542
• 31 Saal J G, Steidie M, Einsele H, Müller C A, Fritz P, Zacher J. Persistence of B 19 parvovirus in synovial membranes of patients with rheumatoid arthritis.  Rheumatol Int. 1992;  12 147-151
• 32 Brown K E. Haematological consequences of parvovirus B 19 infection.  Baillieres Best Pract Res Clin Haematol. 2000;  13 245-259
• 33 Brown K E, Young N S. Parvovirus B 19 in human disease.  Annu Rev Med. 1997;  48 59-67
• 34 Brown K E, Young N S. Parvovirus B 19 infection and hematopoiesis.  Blood Rev. 1995;  9 176-182
• 35 Anderson M J, Higgins P G, Davis L R, Willman J S, Jones S E, Kidd I M, Pattison J R, Tyrrell D A. Experimental parvoviral infection in humans.  J Infect Dis. 1985;  152 257-265
• 36 Nagai K, Morohoshi T, Kudoh T, Yoto Y, Suzuki N, Matsunaga Y. Transient erythroblastopenia of childhood with megakaryocytopenia associated with human parvovirus B 19 infection.  Brit J Hematol. 1992;  80 131-132
• 37 Barlow G D, McKendrick M W. Parvovirus B 19 causing leucopenia and neutropenia in a healthy adult.  J Infect. 2000;  40 192-195
• 38 Scheurlen W, Ramasubbu K, Wachowski O, Hemauer A, Modrow S. Chronic autoimmune thrombopenia / neutropenia in a boy with persistent parvovirus B 19 infection.  J Clin Virol. 2001;  20 173-178
• 39 Kurtzman G J, Ozawa K, Cohen B, Hanson G, Oseas R, Young N S. Chronic bone marrow failure due to persistent B 19 parvovirus infection.  N Engl J Med. 1987;  317 287-294
• 40 Kurtzman G J, Cohen B, Meyers P, Amunullah A, Young N S. Persistent B 19 parvovirus infection as a cause of severe chronic anaemia in children with acute lymphocytic leukaemia.  Lancet. 1988;  2 1159-1162
• 41 Nigro G, Bastianon V, Colloridi V, Ventriglia F, Gallo P, D'Amati G, Koch W C, Adler S P. Human parvovirus B 19 infection in infancy associated with acute and chronic lymphocytic myocarditis and high cytokine levels: report of 3 cases and review.  Clin Infect Dis. 2000;  31 65-69
• 42 Drago F, Semino M, Rampini P, Rebora A. Parvovirus B 19 infection associated with acute hepatitis and a purpuric exanthem.  Br J Dermatol. 1999;  141 160-161
• 43 Karetnyi Y V, Beck P R, Markin R S, Langnas A N, Naides S J. Human parvovirus B 19 infection in acute fulminant liver failure.  Arch Virol. 1999;  144 1713-1724
• 44 Nakazawa T, Tomosugi N, Sakamoto K, Asaka M, Yuri T, Ishikawa I, Kitagawa S. Acute glomerulonephritis after human parvovirus B 19 infection.  Am J Kidney Dis. 2000;  35 E 31
• 45 Komischke K, Searle K, Enders G. Maternal serum alpha-fetoprotein and human chorionic gonadotropin in pregnant women with acute parvovirus B 19 infection with and without fetal complications.  Prenat Diagn. 1997;  17 1039-1046
• 46 Caul E O, Usher M J, Burton P A. Intrauterine infection with human parvovirus B 19: a light and electron microscopy study.  J Med Virol. 1988;  24 55-66
• 47 Bostic J R, Brown K E, Young N S, Koenig S. Quantitative analysis of neutralizing immune responses to human parvovirus B 19 using a novel reverse transcriptase-polymerase chain reaction-based assay.  J Infect Dis. 1999;  179 619-626
• 48 Brown K E, Green S W, Antunez de Mayolo J, Bellanti J A, Smith S D, Smith T J, Young N S. Congenital anaemia after transplacental B 19 parvovirus infection.  Lancet. 1994;  343 895-896
• 49 Foto F, Saag K G, Scharosch L L, Howard E J, Naides S J. Parvovirus B 19-specific DNA in bone marrow from B 19 arthropathy patients: evidence for B 19 virus persistence.  J Infect Dis. 1993;  167 744-748
• 50 Miller E, Fairley C K, Cohen B J, Seng C. Immediate and long term outcome of human parvovirus B 19 infection in pregnancy.  Br J Obstet Gynaecol. 1998;  105 174-178
• 51 Smoleniec J S, Pillai M. Management of fetal hydrops associated with parvovirus B 19 infection.  Br J Obstet Gynaecol. 1994;  101 1079-1081
• 52 Ismail K M, Martin W L, Ghosh S, Whittle M J, Kilby M D. Etiology and outcome of hydrops fetalis.  J Matern Fetal Med. 2001;  10 175-181
• 53 Yaegashi N, Okamura K, Yajima A, Murai C, Sugamura K. The frequency of human parvovirus B 19 infection in nonimmune hydrops fetalis.  J Perinat Med. 1994;  22 159-163
• 54 Jordan J A. Identification of human parvovirus B 19 infection in idiopathic nonimmune hydrops fetalis.  Am J Obstet Gynecol. 1996;  174 37-42
• 55 Yaegashi N. Pathogenesis of nonimmune hydrops fetalis caused by intrauterine B 19 infection.  Tohoku J Exp Med. 2000;  190 65-82
• 56 Yaegashi N, Niinuma T, Chisaka H, Uehara S, Okamura K, Shinkawa O, Tsunoda A, Moffatt S, Sugamura K, Yajima A. Serologic study of human parvovirus B 19 infection in pregnancy in Japan.  J Infect. 1999;  38 30-35
• 57 Enders G, Biber M. Parvovirus B 19 infections in pregnancy. Behring Inst Mitt 1990; 74-78
• 58 Essary L R, Vnencak-Jones C L, Manning S S, Olson S J, Johnson J E. Frequency of parvovirus B 19 infection in nonimmune hydrops fetalis and utility of three diagnostic methods.  Hum Pathol. 1998;  29 696-701
• 59 Forestier F, Tissot J D, Vial Y, Daffos F, Hohlfeld P. Haematological parameters of parvovirus B 19 infection in 13 fetuses with hydrops foetalis.  Br J Haematol. 1999;  104 925-927
• 60 Guidozzi F, Ballot D, Rothberg A D. Human B 19 parvovirus infection in an obstetric population. A prospective study determining fetal outcome.  J Reprod Med. 1994;  39 36-38
• 61 Searle K, Guilliard C, Wallat S, Schalasta G, Enders G. Acute parvovirus B 19 infection in pregnant women - an analysis of serial samples by serological and semi-quantitative PCR techniques.  Infection. 1998;  26 139-143
• 62 Harger J H, Adler S P, Koch W C, Harger G F. Prospective evaluation of 618 pregnant women exposed to parvovirus B 19: risks and symptoms.  Obstet Gynecol. 1998;  91 413-420
• 63 Sheikh A U, Ernest J M, O'Shea M. Long-term outcome in fetal hydrops from parvovirus B 19 infection.  Am J Obstet Gynecol. 1992;  167 337-341
• 64 Schild R L, Bald R, Plath H, Eis-Hubinger A M, Enders G, Hansmann M. Intrauterine management of fetal parvovirus B 19 infection.  Ultrasound Obstet Gynecol. 1999;  13 161-166
• 65 Van Elsacker-Niele A M, Salimans M M, Weiland H T, Vermey-Keers C, Anderson M J, Versteeg J. Fetal pathology in human parvovirus B 19 infection.  Br J Obstet Gynaecol. 1989;  96 768-775
• 66 Markenson G R, Yancey M K. Parvovirus B 19 infections in pregnancy.  Semin Perinatol. 1998;  22 309-317
• 67 Torok T J. Human parvovirus B 19 infections in pregnancy.  Pediatr Infect Dis J. 1990;  9 772-776
• 68 Wattre P, Dewilde A, Subtil D, Andreoletti L, Thirion V. A clinical and epidemiological study of human parvovirus B 19 infection in fetal hydrops using PCR Southern blot hybridization and chemiluminescence detection.  J Med Virol. 1998;  54 140-144
• 69 Rodis J F, Hovick Jr T J, Quinn D L, Rosengren S S, Tattersall P. Human parvovirus infection in pregnancy.  Obstet Gynecol. 1988;  72 733-738
• 70 Morey A L, Ferguson D J, Fleming K A. Ultrastructural features of fetal erythroid precursors infected with parvovirus B 19 in vitro: evidence of cell death by apoptosis.  J Pathol. 1993;  169 213-220
• 71 Gratacos E, Torres P J, Vidal J, Antolin E, Costa J, Jimenez de Anta M T, Cararach V, Alonso P L, Fortuny A. The incidence of human parvovirus B 19 infection during pregnancy and its impact on perinatal outcome.  J Infect Dis. 1995;  171 1360-1363
• 72 Rodis J F, Quinn D L, Gary G W, Anderson L J, Rosengren S, Cartter M L, Campbell W A, Vintzileos A M. Management and outcomes of pregnancies complicated by human B 19 parvovirus infection: a prospective study.  Am J Obstet Gynecol. 1990;  163 1168-1171
• 73 Schwarz T F, Nerlich A, Roggendorf M. Parvovirus B 19 infection in pregnancy. Behring Inst Mitt 1990; 69-73
• 74 Hedrick J. The effects of human parvovirus B 19 and cytomegalovirus during pregnancy.  J Perinat Neonatal Nurs. 1996;  10 30-39
• 75 Brown K E. Human parvovirus epidemiology and clinical manifestations. In: Anderson LJ, Young NS (eds). Human parvovirus B 19. Vol. 20. Karger, Basel 1997; 42-60
• 76 Tolfvenstam T, Papadogiannakis N, Norbeck O, Petersson K, Broliden K. Frequency of human parvovirus B 19 infection in intrauterine fetal death.  Lancet. 2001;  357 1494-1497
• 77 Skjoldebrand-Sparre L, Tolfvenstam T, Papadogiannakis N, Wahren B, Broliden K, Nyman M. Parvovirus B 19 infection: association with third-trimester intrauterine fetal death.  Bjog. 2000;  107 476-480
• 78 Crowley B, Kokai G, Cohen B. Human parvovirus B 19 and fetal death.  Lancet. 2001;  358 1180-1181
• 79 Sebire N J. Choriodecidual inflammatory syndrome (CoDIS) is the leading, and under recognised, cause of early preterm delivery and second trimester miscarriage.  Med Hypotheses. 2001;  56 497-500
• 80 Nunoue T, Kusuhara K, Hara T. Human fetal infection with parvovirus B 19: maternal infection time in gestation, viral persistence and fetal prognosis.  Pediatr Infect Dis J. 2002;  21 1133-1136
• 81 Enders G, Dotsch J, Bauer J, Nutzenadel W, Hengel H, Haffner D, Schalasta G, Searle K, Brown K E. Life-threatening parvovirus B 19-associated myocarditis and cardiac transplantation as possible therapy: two case reports.  Clin Infect Dis. 1998;  26 355-358
• 82 Naides S J, Weiner C P. Antenatal diagnosis and palliative treatment of non-immune hydrops fetalis secondary to fetal parvovirus B 19 infection.  Prenat Diagn. 1989;  9 105-114
• 83 Morey A L, Keeling J W, Porter H J, Fleming K A. Clinical and histopathological features of parvovirus B 19 infection in the human fetus.  Br J Obstet Gynaecol. 1992;  99 566-574
• 84 Weiland H T, Vermey-Keers C, Salimans M M, Fleuren G J, Verwey R A, Anderson M J. Parvovirus B 19 associated with fetal abnormality.  Lancet. 1987;  1 682-683
• 85 Tiessen R G, van Elsacker-Niele A M, Vermeij-Keers C, Oepkes D, van Roosmalen J, Gorsira M C. A fetus with a parvovirus B 19 infection and congenital anomalies.  Prenat Diagn. 1994;  14 173-176
• 86 Harris J W. Parvovirus B 19 for hematologist.  Am J Hematol. 1992;  39 119-130
• 87 Dieck D, Schild R L, Hansmann M, Eis-Hubinger A M. Prenatal diagnosis of congenital parvovirus B 19 infection: value of serological and PCR techniques in maternal and fetal serum.  Prenat Diagn. 1999;  19 1119-1123
• 88 Nguyen Q T, Sifer C, Schneider V, Allaume X, Servant A, Bernaudin F, Auguste V, Garbarg-Chenon A. Novel human erythrovirus associated with transient aplastic anemia.  J Clin Microbiol. 1999;  37 2483-2487
• 89 Heegaard E D, Panum Jensen I, Christensen J. Novel PCR assay for differential detection and screening of erythrovirus B 19 and erythrovirus V 9.  J Med Virol. 2001;  65 362-367
• 90 Carrington D, Gilmore D H, Whittle M J, Aitken D, Gibson A A, Patrick W J, Brown T, Caul E O, Field A M, Clewley J P,. et al . Maternal serum alpha-fetoprotein - a marker of fetal aplastic crisis during intrauterine human parvovirus infection.  Lancet. 1987;  1 433-435
• 91 Johnson D R, Fisher R A, Helwick J J, Murray D L, Patterson M J, Downes F P. Screening maternal serum alpha-fetoprotein levels and human parvovirus antibodies.  Prenat Diagn. 1994;  14 455-458
• 92 Kurtzman G, Frickhofen N, Kimball J, Jenkins D W, Nienhuis A W, Young N S. Pure red-cell aplasia of 10 years' duration due to persistent parvovirus B 19 infection and its cure with immunoglobulin therapy.  N Engl J Med. 1989;  321 519-523
• 93 Kurtzman G J, Cohen B J, Field A M, Oseas R, Blaese R M, Young N S. Immune response to B 19 parvovirus and an antibody defect in persistent viral infection.  J Clin Invest. 1989;  84 1114-1123
• 94 Schwarz T F, Roggendorf M, Hottentrager B, Deinhardt F, Enders G, Gloning K P, Schramm T, Hansmann M. Human parvovirus B 19 infection in pregnancy.  Lancet. 1988;  2 566-567
• 95 Hansmann M, Gembruch U, Bald R. New therapeutic aspects in nonimmune hydrops fetalis based on four hundred and two prenatally diagnosed cases.  Fetal Ther. 1989;  4 29-36
• 96 Berry P J, Gray E S, Porter H J, Burton P A. Parvovirus infection of the human fetus and newborn.  Semin Diagn Pathol. 1992;  9 4-12
• 97 Cameron A D, Swain S, Patrick W J. Human parvovirus B 19 infection associated with hydrops fetalis.  Aust N Z J Obstet Gynaecol. 1997;  37 316-319
• 98 Bousquet F, Segondy M, Faure J M, Deschamps F, Boulot P. B 19 parvovirus-induced fetal hydrops: good outcome after intrauterine blood transfusion at 18 weeks of gestation.  Fetal Diagn Ther. 2000;  15 132-133
• 99 Selbing A, Josefsson A, Dahle L O, Lindgren R. Parvovirus B 19 infection during pregnancy treated with high-dose intravenous gammaglobulin.  Lancet. 1995;  345 660-661
• 100 Alger L S. Toxoplasmosis and parvovirus B 19.  Infect Dis Clin North Am. 1997;  11 55-75
• 101 Kaijigaya S, Fugii H, Field A. et al . Self-assembled B 19 parvovirus capsids, produced in a baculovirus system, are antigenically and immunogenically similar to native virions.  Proc Natl Acad Sci USA. 1991;  88 4646-4650
• 102 Zuffi E, Manaresi E, Gallinella G, Gentilomi G A, Venturoli S, Zerbini M, Musiani M. Identification of an immunodominant peptide in the parvovirus B 19 VP1 unique region able to elicit a long-lasting immune response in humans.  Viral Immunol. 2001;  14 151-158
• 103 Katz V L, McCoy M C, Kuller J A, Hansen W F. An association between fetal parvovirus B 19 infection and fetal anomalies: a report of two cases.  Am J Perinatol. 1996;  13 43-45
• 104 Saint-Martin J, Bonnaud E, Morinet F, Choulot J J, Mensire A. Acute parvovirus myocarditis with fatal outcome.  Pediatrie. 1991;  46 597-599
• 105 Rogers B B, Mark Y, Oyer C E. Diagnosis and incidence of fetal parvovirus infection in an autopsy series: I. Histology.  Pediatr Pathol. 1993;  13 371-379
• 106 Soulie J C. Cardiac involvement in fetal parvovirus B 19 infection.  Pathol Biol (Paris). 1995;  43 416-419
• 107 Maeda H, Shimokawa H, Satoh S, Nakano H, Nunoue T. Nonimmunologic hydrops fetalis resulting from intrauterine human parvovirus B-19 infection: report of two cases.  Obstet Gynecol. 1988;  72 482-485
• 108 Török T J. Human Parvovirus B 19. In: Remington IS, Klein JO (eds). Infectious diseases of the fetus and newborn infant. 4th ed. Saunders, Philadelphia 1995; 668-702
• 109 Adler S P, Manganello A M, Koch W C, Hempfling S H, Best A M. Risk of human parvovirus B 19 infections among school and hospital employees during endemic periods.  J Infect Dis. 1993;  168 361-368