Ballantyne Syndrome and Congenital Anaemia Associated with Parvovirus B19 Infection: Case Report and Review

Abstract

Acute maternal Parvovirus B19 infection affects about 1% of all pregnancies worldwide. Diaplacental transmission of Parvovirus B19 during the second trimester can cause complications like foetal hydrops, premature delivery or foetal loss in about 20–30% of these pregnancies, whereas the majority of maternal infections remain clinically silent. In individual cases, foetoplacental hydrops (of various origins) can trigger a rare form of Preeclampsia in the pregnant woman. The developing maternal oedema in this situation apparently “mirrors” the hydropic state of the foetus. The symptom triad of foetal hydrops, foetoplacental oedema and maternal anasarca defines Ballantyne syndrome. We report a case of Parvovirus-induced Ballantyne syndrome including a 10-year follow-up of mother and child. While the mother recovered rapidly after (preterm) delivery, the infection complicated the first months of life of the neonate. Congenital transfusion-dependent red cell aplasia and cholestatic hepathopathy took a chronic course but resolved under IVIG treatment. Follow-up now finds both the former neonate and the mother entirely recovered. Current knowledge on Ballantyne syndrome as well as perigestational Parvovirus infections including congenital anaemia is briefly reported and pathophysiological hypotheses are discussed.

Zusammenfassung

Akute Infektionen mit Parvovirus B19 betreffen weltweit etwa 1% der Schwangerschaften. Eine diaplazentare Übertragung des Erregers im zweiten Trimenon führt in rund 20–30% der Fälle zu Komplikationen wie Hydrops Fetalis, Frühgeburtlichkeit oder Spätabort, wohingegen die Mehrzahl der maternalen Infektionen klinisch stumm verläuft. ­In Einzelfällen kann ein fetoplazentarer Hydrops (egal welchen Ursprungs) bei der Schwangeren ­eine seltene Form der Präeklampsie auslösen. Maternale Anasarka „spiegeln“ in dieser Situation den Hydrops des Feten. Diese Symptomentrias fetaler Hydrops, Plazentaödem und maternale ­Anasarka definiert das Ballantyne Syndrom. Wir berichten die Kasuistik eines durch Parvovirus induzierten Ballantyne Syndroms einschließlich einer 10-jährigen Nachbeobachtung von Mutter und Kind. Während sich die Mutter nach der ­(vorzeitigen) Entbindung rasch erholte, verlief die Infektion bei dem Frühgeborenen langwierig und kompliziert: Sowohl eine kongenitale, transfusionspflichtige aplastische Anämie als auch eine cholestatische Hepatopathie nahmen einen chronischen Verlauf und bildeten sich erst nach rund einem Jahr unter intravenöser Immunglobulintherapie zurück. In der Nachbeobachtung ist die Erkrankung bei Mutter und Kind folgenlos ausgeheilt. Der Artikel gibt eine Übersicht über den aktuellen Stand des Wissens bezüglich des Ballantyne Syndroms und gestationsassoziierter Parvovirus Infektionen. Pathophysiologische Zusammenhänge und Hypothesen werden diskutiert.

Key words

Ballantyne syndrome - triple edema - mirror syndrome - preeclampsia - fetal hydrops - Parvovirus - congenital anaemia

Schlüsselwörter

Ballantyne Syndrom - Triple-Ödem - Mirror-Syndrom - Präeklampsie - Hydrops fetalis - Parvovirus - kongenitale Anämie

• References

• 1 Ballantyne JW. The diseases and deformities of the foetus: An attempt towards a new system of ante-natal pathology. Oliver & Boyd; Edinburgh: 1892
• 2 Goodlin RC. Impending fetal death in utero due to isoimmunization. The maternal syndrome; report of three cases. Obstet Gynecol 1957; 10: 299
• 3 Hirsch MR, Mark MS. Pseudotoxämia and erythroblastosis. Report of a case. Obstet Gynecol 1964; 24: 47
• 4 Kaiser IH. Ballantyne and triple edema. Am J Obstet Gynecol 1971; 110: 115-120
• 5 O’Driscoll DT. A fluid retention syndrome associated with severe isoimmunization to the Rhesus factor. J Obstet Gynecol Br Emp 1956; 63: 372
• 6 Midgley DY, Harding K. The mirror syndrome. Eur J Obstet Gynecol Reprod Biol 2000; 88: 201-202
• 7 Carbillon L, Oury JF, Guerin JM et al. Clinical biological features of Ballantyne syndrome and the role of placental hydrops. Obstet Gynecol Surv 1997; 52: 310-314
• 8 Dorman SL, Cardwell MS. Ballantyne syndrome caused by a large placental chorioangioma. Am J Obstet Gynecol 1995; 173: 1632-1633
• 9 Gherman RB, Incerpi MH, Wing DA et al. Ballantyne syndrome: is placental ischemia the etiology?. J Matern Fetal Med 1998; 7: 227-229
• 10 Ordorica SA, Marks F, Frieden FJ et al. Aneurysm of the vein of Galen: a new cause for Ballantyne syndrome. Am J Obstet Gynecol 1990; 162: 1166-1167
• 11 Duthie SJ, Walkinshaw SA. Parvovirus associated fetal hydrops: reversal of pregnancy induced proteinuric hypertension by in utero fetal transfusion. Br J Obstet Gynaecol 1995; 102: 1011-1013
• 12 Quagliarello JR, Passalaqua AM, Greco MA et al. Ballantyne’s triple edema syndrome: prenatal diagnosis with ultrasound and maternal renal biopsy findings. Am J Obstet Gynecol 1978; 132: 580-581
• 13 Zaki M, Greenwood C, Redman CWG. The spontaneous reversal of pre-eclampsia associated with parvovirus-induced hydrops and the placental theory of pre-eclampsia: a case report. Br J Obstet Gynaecol 2003; 110: 1125-1126
• 14 Heyborne KD, Porreco RP. Selective fetocide reverses preeclampsia in discordant twins. Am J Obstet Gynecol 2004; 191: 477-480
• 15 Pirhonen JP, Hartgill TW. Spontaneous reversal of mirror syndrome in a twin pregnancy after a single fetal death. Eur J Obstet Gynecol Reprod Biol 2004; 116: 106-107
• 16 Stillman IE, Karumanchi SA. The glomerular injury of preeclampsia. J Am Soc Nephrol 2007; 18: 2281-2284
• 17 Cacciatore B, Tiitinen A, Stenman UH et al. Normal early pregnancy: serum hCG levels and vaginal ultrasonography findings. Br J Obstet Gynaecol 1990; 97: 899-903
• 18 Colwill JR, Machin GA, Popkin JS et al. Acute second trimester EPH (edema/proteinuria/hypertension) gestosis as an indicator of fetal anomaly. Birth Defects Orig Artic Ser 1987; 23: 179-190
• 19 Esterman A, Finlay TH, Dancis J. The effect of hypoxia on term trophoblast: hormone synthesis and release. Placenta 1996; 17: 217-222
• 20 Fox H. Effect of hypoxia on trophoblast in organ culture. A morphologic and autoradiographic study. Am J Obstet Gynecol 1970; 107: 1058-1064
• 21 Li Y, Matsuzaki N, Masuhiro K et al. Trophoblast-derived tumor necrosis factor-alpha induces release of human chorionic gonadotropin using interleukin-6 (IL-6) and IL-6-receptor-dependent system in the normal human trophoblasts. J Clin Endocrinol Metab 1992; 74: 184-191
• 22 Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1: 177-191
• 23 Spong CY, Ghidini A, Dildy GA et al. Elevated second-trimester maternal serum hCG: a marker of inadequate angiogenesis. Obstet Gynecol 1998; 91: 605-608
• 24 Jensen IP, Thorsen P, Jeune B et al. An epidemic of parvovirus B19 in a population of 3,596 pregnant women: a study of sociodemographic and medical risk factors. Br J Obstet Gynaecol 2000; 107: 637-643
• 25 Xu J, Raff TC, Muallem NS et al. Hydrops fetalis secondary to parvovirus B19 infections. J Am Board Fam Pract 2003; 16: 63-68
• 26 Harger JH, Adler SP, Koch WC et al. Prospective evaluation of 618 pregnant women exposed to parvovirus B19: risks and symptoms. Obstet Gynecol 1998; 91: 413-420
• 27 Tolfvenstam T, Papadogiannakis N, Norbeck O et al. Frequency of human parvovirus B19 infection in intrauterine fetal death. Lancet 2001; 357: 1494-1497
• 28 Young NS, Brown KE. Parvovirus B19. N Engl J Med 2004; 350: 586-597
• 29 Dembinski J, Eis-Hübinger AM, Maar J et al. Long term follow up of serostatus after maternofetal parvovirus B19 infection. Arch Dis Child 2003; 88: 219-221
• 30 Nunoue T, Kusuhara K, Hara T. Human fetal infection with parvovirus B19: maternal infection time in gestation, viral persistence and fetal prognosis. Pediatr Infect Dis J 2002; 21: 1133-1136
• 31 Modrow S, Parvovirus B. 19: an infectious agent with various manifestations. Dt Ärzteblatt 2001; 98: 1620
• 32 Brown T, Anand A, Ritchie LD et al. Intrauterine parvovirus infection associated with hydrops fetalis. Lancet 1984; 2: 1033-1034
• 33 Jordan JA. Identification of human parvovirus B19 infection in idiopathic nonimmune hydrops fetalis. Am J Obstet Gynecol 1996; 174: 37-42
• 34 Miller E, Fairley CK, Cohen BJ et al. Immediate and long term outcome of human parvovirus B19 infection in pregnancy. Br J Obstet Gynaecol 1998; 105: 174-178
• 35 Rodis JF, Quinn DL, Gary GW et al. Management and outcomes of pregnancies complicated by human B19 parvovirus infection: a prospective study. Am J Obstet Gynecol 1990; 163: 1168-1171
• 36 Pryde PG, Nugent CE, Pridjian G et al. Spontaneous resolution of nonimmune hydrops fetalis secondary to human parvovirus B19 infection. Obstet Gynecol 1992; 79: 859-861
• 37 Brown KE, Green SW, de Mayolo JA et al. Congenital anaemia after transplacental B19 parvovirus infection. Lancet 1994; 343: 895-896
• 38 Schild RL, Bald R, Plath H et al. Intrauterine management of fetal parvovirus B19 infection. Ultrasound Obstet Gynecol 1999; 13: 161-166
• 39 Sheikh AU, Ernest JM, O’Shea M. Long-term outcome in fetal hydrops from parvovirus B19 infection. Am J Obstet Gynecol 1992; 167: 337-341
• 40 Fairley CK, Smoleniec JS, Caul OE et al. Observational study of effect of intrauterine transfusions on outcome of fetal hydrops after parvovirus B19 infection. Lancet 1995; 346: 1335-1337
• 41 Krapp M, Gembruch U. Perinatales Management bei Verdacht auf fetale Anämie. Geburtsh Frauenheilk 2001; 61: 721-723
• 42 Smoleniec JS, Pillai M. Management of fetal hydrops associated with parvovirus B19 infection. Br J Obstet Gynaecol 1994; 101: 1079-1081
• 43 Smith-Whitley K, Zhao H, Hodinka RL et al. Epidemiology of human parvovirus B19 in children with sickle cell disease. Blood 2004; 103: 422-427
• 44 Matsuda H, Sakaguchi K, Shibasaki T et al. Intrauterine therapy for parvovirus B19 infected symptomatic fetus using B19 IgG-rich high titer gammaglobulin. J Perinat Med 2005; 33: 561-563
• 45 Nagel HTC, de Haan TR, Vandenbussche FPHA et al. Long-term outcome after fetal transfusion for hydrops associated with parvovirus B19 infection. Obstet Gynecol 2007; 109: 42-47
• 46 Rodis JF, Rodner C, Hansen AA et al. Long-term outcome of children following maternal human parvovirus B19 infection. Obstet Gynecol 1998; 91: 125-128
• 47 Heegaard ED, Hasle H, Skibsted L et al. Congenital anemia caused by parvovirus B19 infection. Pediatr Infect Dis J 2000; 19: 1216-1218
• 48 Vepreková L, Jelínek J, Zeman J. Congenital aplastic anemia caused by parvovirus B19 infection. Cas Lek Cesk 2001; 140: 178-180
• 49 Forestier F, Tissot JD, Vial Y et al. Haematological parameters of parvovirus B19 infection in 13 fetuses with hydrops foetalis. Br J Haematol 1999; 104: 925-927
• 50 Donders GG, Van Lierde S, Van Elsacker-Niele AM et al. Survival after intrauterine parvovirus B19 infection with persistence in early infancy: a two-year follow-up. Pediatr Infect Dis J 1994; 13: 234-236
• 51 Stepan H, Faber R. Elevated sFlt1 level and preeclampsia with parvovirus-induced hydrops. N Engl J Med 2006; 354: 1857-1858