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Benirschke's Pathology of the Human Placenta pp 633–667Cite as

Erythroblastosis Fetalis, Hydrops Fetalis, and Transplacental Hemorrhage

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Abstract

This chapter reviews the various conditions associated with hydrops fetalis. It aims to familiarize the pathologist with the clinical presentation and evaluation of the maternal-fetal dyad, in addition to key features associated with these conditions on pathologic examination of the fetus and placenta. The pathophysiology of hydrops is discussed as clinically relevant. A better understanding of these entities can help pathologists and clinicians work together to understand the cause of this condition and implications for future pregnancy in an individual case.

These entities are categorized as “immune-mediated” and “nonimmune” hydrops. This distinction reflects the historic importance of hemolytic disease of the fetus and newborn (“immune-mediated” hydrops) as the major disease to be considered leading to tragic recurrent pregnancy loss with hydrops. “Erythroblastosis fetalis” is the term used to describe the hydropic fetus afflicted by hemolytic disease of the fetus and newborn. Since the advent of Rh testing and Rh-immunoglobulin administration to Rh-negative women that could form potential alloantibodies, this disease has fortunately become rare in many nations. Fetal anemia, due to intrinsic abnormalities of erythrocytes, infection, or fetal-maternal hemorrhage, remains a major cause of hydrops to be considered worldwide; this topic is given detailed attention. The various other conditions causing hydrops often relate to abnormal chromosomes, congenital anomalies (especially cardiac defects and lymphatic malformations), arrhythmia, masses in the thorax or abdomen, richly vascular tumors, infections, and inborn errors of metabolism. Other immune-related disorders that can present with fetal hydrops, such as hemophagocytic lymphohistiocytosis, and gestational alloimmune liver disease are also discussed. Familiarization with these rare entities, especially those with recurrent potential, is critical for optimal care.

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References

  1. Abdelkader MA, Ramadan W, Gabr AA, Kamel A, Abdelrahman RW. Fetal intracranial hemorrhage: sonographic criteria and merits of prenatal diagnosis. J Matern Fetal Neonatal Med. 2016;30:2250–6.

    PubMed  Google Scholar 

  2. American College of Obstetricians and Gynecologists' Committee on Practice Bulletins—Obstetrics. ACOG practice bulletin no. 192: management of alloimmunization during pregnancy. Obstet Gynecol. 2018;131(3):e82–90.

    Google Scholar 

  3. Alenghat E, Esterly JR. Intravascular hematopoiesis in chorionic villi. Am J Clin Pathol. 1983;79(2):225–7.

    Google Scholar 

  4. Alexander F, Campbell WA. Congenital nephrotic syndrome and renal vein thrombosis in infancy. J Clin Pathol. 1971;24:27–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Altmann J, Kiver V, Henrich W, Weichert A. Clinical outcome of prenatally suspected cardiac rhabdomyomas of the fetus. J Perinat Med. 2019;48:74–81.

    PubMed  Google Scholar 

  6. Anandakumar C, Biswas A, Chew SSL, Chia D, Wong YC, Ratnam SS. Direct fetal therapy for hydrops secondary to congenital atrioventricular heart block. Obstet Gynecol. 1996;87:835–7.

    CAS  PubMed  Google Scholar 

  7. Anders D, Kindermann G, Pfeifer U. Metastasizing fetal neuroblastoma with involvement of the placenta simulating fetal erythroblastosis. J Pediatr. 1973;82:50–3.

    CAS  PubMed  Google Scholar 

  8. Ashshi A, Cooper RJ, Klapper PE, Al-Jiffri O, Moore L. Detection of human herpes virus 6 DNA in fetal hydrops. Lancet. 2000;355:1519–20.

    CAS  PubMed  Google Scholar 

  9. Aslam PA, Korones SB, Richardson RL, Pate JW. Congenital cystic adenomatoid malformation with anasarca. JAMA. 1970;212:622–4.

    CAS  PubMed  Google Scholar 

  10. Aydinok Y. Thalassemia. Hematology. 2012;17(Suppl 1):S28–31.

    CAS  PubMed  Google Scholar 

  11. Bachmann KD, Kröll W. Über das prenatal entstandene neuroblastoma sympathicum. Z Kinderheilk. 1968;103:61–72.

    CAS  PubMed  Google Scholar 

  12. Ballantyne JW. Diseases and deformities of the fetus, vol. 1. Edinburgh: Oliver & Boyd; 1892.

    Google Scholar 

  13. Bard H, Prosmanne J. Relative rates of fetal hemoglobin and adult hemoglobin synthesis in cord blood of infants of insulin-dependent diabetic mothers. Pediatrics. 1985;75:1143–7.

    CAS  PubMed  Google Scholar 

  14. Barron SD, Pass RF. Infectious causes of hydrops fetalis. Semin Perinatol. 1995;19:493–501.

    CAS  PubMed  Google Scholar 

  15. Baschat AA, Harman CR, Alger LS, Weiner CP. Fetal coronary and cerebral blood flow in acute fetomaternal hemorrhage. Ultrasound Obstet Gynecol. 1998;12:128–31.

    CAS  PubMed  Google Scholar 

  16. Batstone GF, Golde DJ, Letchworth AT, McIver A. Congenital (Finnish) nephrosis as cause of abnormal amniotic fluid alpha-protein. Lancet. 1981;i:664.

    Google Scholar 

  17. Battaglia FC, Woolever CA. Fetal and neonatal complications associated with recurrent chorioangiomas. Pediatrics. 1968;41:62–6.

    CAS  PubMed  Google Scholar 

  18. Bawle EV, Black V. Nonimmune hydrops fetalis in Noonan’s syndrome. Am J Dis Child. 1986;140:758–60.

    CAS  PubMed  Google Scholar 

  19. Beck M, Bender SW, Reiter HL, Otto W, Bässler R, Dancygier H, Gehler J. Neuraminidase deficiency presenting as non-immune hydrops fetalis. Eur J Pediatr. 1984;143:135–9.

    CAS  PubMed  Google Scholar 

  20. Becker V, Bleyl U. Placentarzotte bei Schwangerschaftstoxikose und fetaler Erythroblastose im fluorescenzmikroskopischen Bilde. Virchows Arch Pathol Anat. 1961;334:516–27.

    CAS  Google Scholar 

  21. Beischer NA, Holsman M, Kitchen WH. Relation of various forms of anemia to placental weight. Am J Obstet Gynecol. 1968;101:801–9.

    CAS  PubMed  Google Scholar 

  22. Bellini C, Fulcheri E, Rutigliani M, Calevo MG, Boccardo F, Campisi C, Bonioli E, Bellini T, Hennekam RC. Immunohistochemistry in non-immune hydrops fetalis: a single center experience in 79 fetuses. Am J Med Genet A. 2010;152A:1189–96.

    PubMed  Google Scholar 

  23. Bellini C, Donarini G, Paladini D, Calevo MG, Bellini T, Ramenghi LA, Hennekam RC. Etiology of non-immune hydrops fetalis: an update. Am J Med Genet A. 2015;167A:1082–8.

    PubMed  Google Scholar 

  24. Bellussi F, Perolo A, Ghi T, Youssef A, Pilu G, Simonazzi G. Diagnosis of severe fetomaternal hemorrhage with fetal cerebral Doppler: case series and systematic review. Fetal Diagn Ther. 2017;41:1–7.

    PubMed  Google Scholar 

  25. Benacerraf BR, Frigoletto FD. In utero treatment of a fetus with diaphragmatic hernia complicated by hydrops. Am J Obstet Gynecol. 1986;155:817–8.

    CAS  PubMed  Google Scholar 

  26. Ben-Ami M, Shalev E, Romano S, Zuckerman H. Midtrimester diagnosis of endocardial fibroelastosis and atrial septal defect: a case report. Am J Obstet Gynecol. 1986;155:662–3.

    CAS  PubMed  Google Scholar 

  27. Benirschke K, Swartz WH, Leopold G, Sahn D. Hydrops due to myocarditis in a fetus. Am J Cardiovasc Pathol. 1986;1:131–3.

    Google Scholar 

  28. Berkowitz RL, Chitkara U, Goldberg JD, Wilkins I, Chervenak FA, Lynch L. Intrauterine intravascular transfusions for severe red blood cell isoimmunization: ultrasound-guided percutaneous approach. Am J Obstet Gynecol. 1986;155:574–81.

    CAS  PubMed  Google Scholar 

  29. Biankin SA, Arbuckle SM, Graf NS. Autopsy findings in a series of five cases of fetomaternal haemorrhages. Pathology. 2003;35:319–24.

    PubMed  Google Scholar 

  30. Birkenfeld A, Mordel N, Okon E. Direct demonstration of iron in a term placenta in a case of β-thalassemia. Am J Obstet Gynecol. 1989;160:562–3.

    CAS  PubMed  Google Scholar 

  31. Birner WF. Neuroblastoma as a cause of antenatal death. Am J Obstet Gynecol. 1961;82:1388–91.

    CAS  PubMed  Google Scholar 

  32. Boehm CD, Antonakarakis SE, Phillips JA III, Stetten G, Kazazian HH. Prenatal diagnosis using DNA polymorphisms. Report on 95 pregnancies at risk for sickle-cell disease or β-thalassemia. N Engl J Med. 1983;308:1054–8.

    CAS  PubMed  Google Scholar 

  33. Bouissou H, Kanoun T, Bierme S, Bierme R. Foie et placenta au cours de la maladie hémolytique par iso-immunisation Rh. (Étude histologique et déductions). Pathol Biol. 1969;17:109–20.

    CAS  PubMed  Google Scholar 

  34. Braun T, Brauer M, Fuchs I, Czernik C, Dudenhausen JW, Henrich W, Sarioglu N. Mirror syndrome: a systematic review of fetal associated conditions, maternal presentation and perinatal outcome. Fetal Diagn Ther. 2010;27:191–203.

    PubMed  Google Scholar 

  35. Bridge JA, McManus BM, Remmenga J, Cuppage FP. Complete heart block in the 18p- syndrome. Congenital calcification of the atrioventricular node. Arch Pathol Lab Med. 1989;113:539–41.

    CAS  PubMed  Google Scholar 

  36. Brinson RA, Goldsmith JP. Nonimmune hydrops fetalis associated with intrauterine intussusception. J Perinatol. 1988;8:225–7.

    CAS  PubMed  Google Scholar 

  37. Broderick K, Oyer R, Chatwani A. Neu-Laxova syndrome: a case report. Am J Obstet Gynecol. 1988;158:574–5.

    CAS  PubMed  Google Scholar 

  38. Bromley B, Frigoletto FD, Estroff JA, Benacerraf BR. The natural history of oligohydramnios/polyhydramnios sequence in monochorionic diamniotic twins. Ultrasound Obstet Gynecol. 1992;2:317–20.

    CAS  PubMed  Google Scholar 

  39. Burger K. Mit Hydrops foetus et placentae einhergehende Luteinzysten. Zbl Gynäkol. 1947;69:533–6.

    Google Scholar 

  40. Burstein RH, Blumenthal HT. Vascular lesions of the placenta of possible immunogenic origin in erythroblastosis fetalis. Am J Obstet Gynecol. 1962;83:1062–8.

    CAS  PubMed  Google Scholar 

  41. Busch W, Vogel M. Die Plazenta beim “Morbus haemolyticus neonatorum”. Z Geburtshilfe Perinatol. 1972;176:17–28.

    CAS  PubMed  Google Scholar 

  42. Burwick RM, Pilliod RA, Dukhovny SE, Caughey AB. Fetal hydrops and the risk of severe preeclampsia. J Matern Fetal Neonatal Med. 2019;32(6):961–5.

    PubMed  Google Scholar 

  43. Cantu-Rajnoldi A, Zanella A, Conter U, Faccini P, Soligo D, Gornati G, Vegni C, Nicolini U. A severe transfusion-dependent congenital dyserythropoietic anemia presenting as hydrops fetalis. Br J Haematol. 1997;96:530–3.

    CAS  PubMed  Google Scholar 

  44. Carles D, André G, Pelluard F, Martin O, Sauvestre F. Pathological findings in feto-maternal hemorrhage. Pediatr Dev Pathol. 2014;17:102–6.

    PubMed  Google Scholar 

  45. Carles D, Serville F, Dubecq J-P, Alberti EM, Horowitz J, Weichwold W. Idiopathic arterial calcification in a stillborn complicated by pleural hemorrhage and hydrops fetalis. Arch Pathol Lab Med. 1992;116:293–5.

    CAS  PubMed  Google Scholar 

  46. Carpenter RJ Jr, Strasburger JF, Garson A Jr, Smith RT, Deter RL, Engelhardt HT Jr. Fetal ventricular pacing for hydrops secondary to complete atrioventricular block. J Am Coll Cardiol. 1986;8:1434–6.

    PubMed  Google Scholar 

  47. Carr S, Rubin L, Dixon D, Star J, Dailey J. Intrauterine therapy for homozygous α-thalassemia. Obstet Gynecol. 1995;85:876–9.

    CAS  PubMed  Google Scholar 

  48. Carter BS, DiGiacomo JE, Balderston SM, Wiggins JW, Merenstein GB. Disproportionate septal hypertrophy associated with erythroblastosis. Am J Dis Child. 1990;144:1225–8.

    CAS  PubMed  Google Scholar 

  49. Catanzarite VA, Schrimmer DB, Maida C, Mendoza A. Prenatal sonographic diagnosis of intracranial haemorrhage: report of a case with a sinusoidal fetal heart rate tracing, and review of the literature. Prenat Diagn. 1995;15:229–35.

    CAS  PubMed  Google Scholar 

  50. Chaudet K, Kaimal A, Deshpande V, Roberts DJ. INI1 negative sarcoma diagnosed as malignant rhabdoid tumor presenting as hydrops fetalis metastatic to the placenta: a case report and review of the literature on congenital sarcomas. J Matern Fetal Neonatal Med. 2019;12:1–4.

    Google Scholar 

  51. Chelliah BP, Cabatu E, Chitkara U, Krousop RW, Ainbender E, Brown EG. Polyhydramnios and elevated amniotic fluid alpha-fetoprotein caused by fetal supraventricular tachycardia. J Reprod Med. 1981;26:45–7.

    CAS  PubMed  Google Scholar 

  52. Chen C, Tan J, Wang L, Han B, Sun W, Zhao L, Huang C, Tan B, Qin L. Unexpected red blood cell antibody distributions in Chinese people by a systematic literature review. Transfusion. 2016;56:975–9.

    CAS  PubMed  Google Scholar 

  53. Chitayat D, Gruber H, Mullen BJ, Pauzner D, Costa T, Lachman R, Rimoin DL. Hydrops-ectopic calcification-moth-eaten skeletal dysplasia (Greenberg dysplasia): prenatal diagnosis and further delineation of a rare genetic disorder. Am J Med Genet. 1993;47:272–7.

    CAS  PubMed  Google Scholar 

  54. Choi D, Schroer SA, Lu SY, Wang L, Wu X, Liu Y, Zhang Y, Gaisano HY, Wagner KU, Wu H, Retnakaran R, Woo M. Erythropoietin protects against diabetes through direct effects on pancreatic beta cells. J Exp Med. 2010;207(13):2831–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Choi YJ, Saba JD. Sphingosine phosphate lyase insufficiency syndrome (SPLIS): a novel inborn error of sphingolipid metabolism. Adv Biol Regul. 2019;71:128–40.

    CAS  PubMed  Google Scholar 

  56. Chon AH, Korst LM, Abdel-Sattar M, Llanes A, Ouzounian JG, Chmait RH. Types II and III congenital pulmonary airway malformation with hydrops treated in utero with percutaneous sclerotherapy. Prenat Diagn. 2018;38:493–8.

    CAS  PubMed  Google Scholar 

  57. Christensen RD, Lambert DK, Baer VL, Richards DS, Bennett ST, Ilstrup SJ, Henry E. Severe neonatal anemia from fetomaternal hemorrhage: report from a multihospital health-care system. J Perinatol. 2013;33:429–34.

    CAS  PubMed  Google Scholar 

  58. Christie RW. Lutein cysts of ovaries associated with erythroblastotic hydrops fetalis. Assay of gonadotropin in serum of Rh-sensitized women in later stages of pregnancy. Am J Clin Pathol. 1961;36:518–23.

    CAS  PubMed  Google Scholar 

  59. Chui DH. Alpha-thalassemia: Hb H disease and Hb Barts hydrops fetalis. Ann N Y Acad Sci. 2005;1054:25–32.

    CAS  PubMed  Google Scholar 

  60. Clark SL, Vitale DJ, Minton SD, Stoddard RA, Sabey PL. Successful fetal therapy for cystic adenomatoid malformation associated with second-trimester hydrops. Am J Obstet Gynecol. 1987;157:294–5.

    CAS  PubMed  Google Scholar 

  61. Clausen FB, Hellberg Å. External quality assessment of noninvasive fetal RHD genotyping. Vox Sang. 2020;115:466–71.

    CAS  PubMed  Google Scholar 

  62. Collins JH. Prenatal observation of umbilical cord torsion with subsequent premature labor and delivery of a 31-week infant with mild nonimmune hydrops. Am J Obstet Gynecol. 1995;172:1048–9.

    CAS  PubMed  Google Scholar 

  63. Copel JA, Buyon JP, Kleinman CS. Successful in utero therapy of fetal heart block. Am J Obstet Gynecol. 1995;173:1384–90.

    CAS  PubMed  Google Scholar 

  64. Collardeau-Frachon S, Heissat S, Bouvier R, Fabre M, Baruteau J, Broue P, Cordier MP, Debray D, Debiec H, Ronco P, Guigonis V. French retrospective multicentric study of neonatal hemochromatosis: importance of autopsy and autoimmune maternal manifestations. Pediatr Dev Pathol. 2012;15:450–70.

    CAS  PubMed  Google Scholar 

  65. Cox PM, Brueton LA, Murphy KW, Worthington VC, Bjelorglic P, Lazda EJ, Sabire NJ, Sewry CA. Early-onset fetal hydrops and muscle degeneration in siblings due to a novel variant of type IV glycogenosis. Am J Med Genet. 1999;86:187–93.

    CAS  PubMed  Google Scholar 

  66. Croonen EA, Nillesen WM, Stuurman KE, Oudesluijs G, van de Laar IM, Martens L, Ockeloen C, Mathijssen IB, Schepens M, Ruiterkamp-Versteeg M, Scheffer H, Faas BH, van der Burgt I, Yntema HG. Prenatal diagnostic testing of the Noonan syndrome genes in fetuses with abnormal ultrasound findings. Eur J Hum Genet. 2013;21:936–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Crowley MA, Mollan TL, Abdulmalik OY, Butler AD, Goodwin EF, Sarkar A, Stolle CA, Gow AJ, Olson JS, Weiss MJ. A hemoglobin variant associated with neonatal cyanosis and anemia. N Engl J Med. 2011;364:1837–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Cukierski MA, Tarantal AF, Hendrickx AG. A case of nonimmune hydrops fetalis with a rare cardiac anomaly in a rhesus monkey. J Med Primatol. 1986;15:227–34.

    CAS  PubMed  Google Scholar 

  69. Cumming DC. Recurrent nonimmune hydrops fetalis. Obstet Gynecol. 1979;54:124–6.

    CAS  PubMed  Google Scholar 

  70. Curry CJR, Chopra D, Finer NN. Hydrops and pleural effusions in congenital myotonic dystrophy. J Pediatr. 1988;113:555–7.

    CAS  PubMed  Google Scholar 

  71. Dana M, Fibach E. Elimination of ABO blood group incompatible fetal red blood cells in the maternal circulation: relevance to the diagnosis of fetal-maternal hemorrhage. Neonatology. 2018;114:303–6.

    CAS  PubMed  Google Scholar 

  72. DeLia JE, Emery MG. Digoxin therapy in the fetus. Am J Dis Child. 1986;140:974–5.

    CAS  Google Scholar 

  73. Devi B, Jennison RF, Langley FA. Significance of placental pathology in transplacental haemorrhage. J Clin Pathol. 1968;21:322–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Doss BJ, Vicari J, Jacques SM, Qureshi F. Placental involvement in congenital hepatoblastoma. Pediatr Dev Pathol. 1998;1:538–42.

    CAS  PubMed  Google Scholar 

  75. Driscoll SG, Steinke J. Pancreatic insulin content in severe erythroblastosis fetalis. Pediatrics. 1967;39:449–50.

    Google Scholar 

  76. Drut RM, Drut R. Nonimmune fetal hydrops and placentomegaly: diagnosis of familial Wiedemann-Beckwith syndrome with trisomy 11p15 using FISH. Am J Med Genet. 1996;62:145–9.

    CAS  PubMed  Google Scholar 

  77. Ek S, Rosenborg S. Mesalazine as a cause of fetal anemia and hydrops fetalis: a case report. Medicine (Baltimore). 2017;96:e9277. Published correction appears in Medicine (Baltimore). 2018 97:e9623.

    PubMed  Google Scholar 

  78. Espinoza J, Romero R, Nien JK, Kusanovic JP, Richani K, Gomez R, Kim CJ, Mittal P, Gotsh F, Erez O, Chaiworapongsa T, Hassan S. A role of the anti-angiogenic factor sVEGFR-1 in the 'mirror syndrome' (Ballantyne's syndrome). J Matern Fetal Neonatal Med. 2006;19:607–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Fan M, Skupski DW. Placental chorioangioma: literature review. J Perinat Med. 2014;42:273–9.

    PubMed  Google Scholar 

  80. Fenjves ES, Ochoa MS, Cabrera O, Mendez AJ, Kenyon NS, Inverardi L, Ricordi C. Human, nonhuman primate, and rat pancreatic islets express erythropoietin receptors. Transplantation. 2003;75:1356–60.

    CAS  PubMed  Google Scholar 

  81. Fotiou E, Martin-Almedina S, Simpson MA, Lin S, Gordon K, Brice G, Atton G, Jeffery I, Rees DC, Mignot C, Vogt J, Homfray T, Snyder MP, Rockson SG, Jeffery S, Mortimer PS, Mansour S, Ostergaard P. Novel mutations in PIEZO1 cause an autosomal recessive generalized lymphatic dysplasia with non-immune hydrops fetalis. Nat Commun. 2015;6:8085. Erratum in: Nat Commun. (2019) 10:1951.

    PubMed  Google Scholar 

  82. Fox H. The incidence and significance of nucleated erythrocytes in the foetal vessels of the mature human placenta. J Obstet Gynaecol Br Commonw. 1967;74:40–3.

    CAS  PubMed  Google Scholar 

  83. Friedman S, Ford-Jones LE, Toi A, Ryan G, Blaser S, Chitayat D. Congenital toxoplasmosis: prenatal diagnosis, treatment and postnatal outcome. Prenat Diagn. 1999;19:330–3.

    CAS  PubMed  Google Scholar 

  84. Friesen RF, Bowman JM, Barnes PH, Grewar D, Mcinnis C, Bowman WD. Intrauterine transfusions for erythroblastosis. Am J Obstet Gynecol. 1967;97:343–9.

    CAS  PubMed  Google Scholar 

  85. Fucharoen S, Winichagoon P, Wisedpanichkij R, Sae-Ngow B, Sriphanich R, Oncoung W, Muangsapaya W, Chowthaworn J, Kanokpongsakdi S, Bunyaratvej A, Piankijagum A, Dewaele C. Prenatal and postnatal diagnoses of thalassemias and hemoglobinopathies by HPLC. Clin Chem. 1998;44:740–8.

    CAS  PubMed  Google Scholar 

  86. Fung TY, Fung YMH, Ng PC, Yeung CK, Chang MZA. Polyhydramnios and hypercalcemia associated with congenital mesoblastic nephroma: case report and a new appraisal. Obstet Gynecol. 1995;85:815–7.

    CAS  PubMed  Google Scholar 

  87. Gallagher PG, Weed SA, Tse WT, Benoit L, Morrow JS, Marchesi SL, Mohandas N, Forget BG. Recurrent fatal hydrops fetalis associated with a nucleotide substitution in the erythrocyte β-spectrin gene. J Clin Invest. 1995;95:1174–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Gambale A, Iolascon A, Andolfo I, Russo R. Diagnosis and management of congenital dyserythropoietic anemias. Expert Rev Hematol. 2016;9(3):283–96. https://doi.org/10.1586/17474086.2016.1131608.

    Article  CAS  PubMed  Google Scholar 

  89. Geaghan SM. Diagnostic laboratory technologies for the fetus and neonate with isoimmunization. Semin Perinatol. 2011;35:148–54.

    PubMed  Google Scholar 

  90. Gautier E, Benachi A, Giovangrandi Y, Ernault P, Olivi M, Gaillon T, Costa J-M. Fetal RhD genotyping by maternal serum analysis: a two-year experience. Am J Obstet Gynecol. 2005;192:666–9.

    CAS  PubMed  Google Scholar 

  91. Geifman-Holtzman O, Grotegut CA, Gaughan JP. Diagnostic accuracy of noninvasive Rh genotyping from maternal blood – a meta-analysis. Am J Obstet Gynecol. 2006;195:1163–73.

    PubMed  Google Scholar 

  92. Gembruch U, Niesen M, Hansmann M, Knöpple G. Listeriosis: a cause of non-immune hydrops fetalis. Prenat Diagn. 1987;7:277–82.

    CAS  PubMed  Google Scholar 

  93. Giacoia GP. Severe fetomaternal hemorrhage: a review. Obstet Gynecol Surv. 1997;52:372–80.

    CAS  PubMed  Google Scholar 

  94. Giles HM, Pugh RCB, Darmady EM, Stranack F, Woolf LI. The nephrotic syndrome in early infancy: a report of three cases. Arch Dis Child. 1957;32:167–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Gillan JE, Lowden JA, Gaskin K, Cutz E. Congenital ascites as a presenting sign of lysosomal storage disease. J Pediatr. 1984;104:225–31.

    CAS  PubMed  Google Scholar 

  96. Ginsburg SJ, Groll M. Hydrops fetalis due to infantile Gaucher’s disease. J Pediatr. 1973;82:1046–8.

    CAS  PubMed  Google Scholar 

  97. Gloster ES, Jimenez JF, Godoy G, Burrows P, Hill D, Mollitt DL, Grunow WA. Nonimmune hydrops fetalis: the Arkansas Children’s Hospital experience for 1982–1983. Lab Investig. 1984;50:3P.

    Google Scholar 

  98. Godra A, Kim DU, D’Cruz C. A 5-day-old boy with hydrops fetalis. Arch Pathol Lab Med. 2003;127:1051–2.

    PubMed  Google Scholar 

  99. Gonen R, Fong K, Chiasson DA. Prenatal sonographic diagnosis of hepatic hemangioendothelioma with secondary nonimmune hydrops fetalis. Obstet Gynecol. 1989;73:485–7.

    CAS  PubMed  Google Scholar 

  100. Gonsoulin W, Copeland KL, Carpenter RJ, Hughes MR, Elder FB. Fetal blood sampling demonstrating chimerism in monozygotic twins discordant for sex and tissue karyotype (46, XY and 45, X). Prenat Diagn. 1990;10:25–8.

    CAS  PubMed  Google Scholar 

  101. Gottschalk W, Abramson D. Placental edema and fetal hydrops. A case of congenital cystic and adenomatoid malformation of the lung. Obstet Gynecol. 1957;10:626–31.

    CAS  PubMed  Google Scholar 

  102. Grannum PAT, Copel JA, Moya FR, Scioscia AL, Robert JA, Winn HN, Coster BC, Burdine CB, Hobbins JC. The reversal of hydrops fetalis by intravascular intrauterine transfusion in severe isoimmune fetal anemia. Am J Obstet Gynecol. 1988;158:914–9.

    CAS  PubMed  Google Scholar 

  103. Gray ES. Mesoblastic nephroma and non-immunological hydrops fetalis. Letter to the editor. Pediatr Pathol. 1989;9:607–9.

    CAS  PubMed  Google Scholar 

  104. Green DW, Donovan EF, Wood BP. Radiological case of the month. Hydrops fetalis with pulmonary hypoplasia. Am J Dis Child. 1990;144:93–4.

    CAS  PubMed  Google Scholar 

  105. Greenberg F, Carpenter RJ, Ledbetter DH. Cystic hygroma and hydrops fetalis in a fetus with trisomy 13. Clin Genet. 1983;24:389–91.

    CAS  PubMed  Google Scholar 

  106. Greenberg F, Faucett A, Rose E, Bancalari L, Kardon NB, Mizejewski G, Haddon JE, Alpert E. Congenital deficiency of α-fetoprotein. Am J Obstet Gynecol. 1992;167:509–11.

    CAS  PubMed  Google Scholar 

  107. Gropp A. Chapter 8: Fetal hydrops in chromosome disorders as principle of damage in developmental pathology. Clinical observations in man and experimental studies in the mouse. In: Ryder OA, Byrd ML, editors. One medicine. New York: Springer; 1984. p. 84–95.

    Google Scholar 

  108. Groves GR, Baskett TF. Nonimmune hydrops fetalis: antenatal diagnosis and management. Am J Obstet Gynecol. 1984;148:563–9.

    Google Scholar 

  109. Grootenboer-Mignot S, Crétien A, Laurendeau I, Poissonnier MH, Doireau V, Brossard Y, Tchernia G, Cynober T, Delaunay J. Sub-lethal hydrops as a manifestation of dehydrated hereditary stomatocytosis in two consecutive pregnancies. Prenat Diagn. 2003;23:380–4.

    CAS  PubMed  Google Scholar 

  110. Guntheroth WG, Cyr DR, Mack LA, Benedetti T, Lenke RR, Petty CN. Hydrops from reciprocating atrioventricular tachycardia in a 27-week fetus requiring quinidine for conversion. Obstet Gynecol. 1985;66:29S–33S.

    CAS  PubMed  Google Scholar 

  111. Guy G, Coady DJ, Jansen V, Snyder J, Zinberg S. α-Thalassemia hydrops fetalis: clinical and ultrasonographic considerations. Am J Obstet Gynecol. 1985;153:500–4.

    CAS  PubMed  Google Scholar 

  112. Hallak M, Neerhof MG, Perry R, Nazir M, Hulka JC. Fetal supraventricular tachycardia and hydrops fetalis: combined intensive, direct, and transplacental therapy. Obstet Gynecol. 1991;78:523–5.

    CAS  PubMed  Google Scholar 

  113. Halvorsen S, Bechensteen AG. Physiology of erythropoietin during mammalian development. Acta Paediatr Suppl. 2002;91:17–26.

    CAS  PubMed  Google Scholar 

  114. Hannah DM, Tressler TB, Taboada CD. Nonimmune hydrops fetalis due to autosomal recessive hereditary spherocytosis. Case Rep Womens Health. 2017;16:4–7. Published 2017 Oct 2. https://doi.org/10.1016/j.crwh.2017.09.003.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Hardy L, Hansen JL, Kushner JP, Knisely AS. Neonatal hemochromatosis. Genetic analysis of transferrin-receptor, H-apoferritin, and L-apoferritin loci and of the human leukocyte antigen class I region. Am J Pathol. 1991;137:149–53.

    Google Scholar 

  116. Harkavy KL, Scanlon JW. Hydrops fetalis in a parabiotic, acardiac twin. Am J Dis Child. 1978;132:638–9.

    Google Scholar 

  117. Harman CR, Bowman JM, Menticoglou SM, Pollock JM, Manning FA. Profound fetal thrombocytopenia in rhesus disease: serious hazard at intravascular transfusion. Lancet. 1988;2(8613):741–2.

    CAS  PubMed  Google Scholar 

  118. Harper DC, Swingle HM, Weiner CP, Bonthius DJ, Aylward GP, Widness JA. Long-term neurodevelopmental outcome and brain volume after treatment for hydrops fetalis by in utero intravascular transfusion. Am J Obstet Gynecol. 2006;195:192–200.

    PubMed  Google Scholar 

  119. Harrigan JT, Kangos JJ, Sikka A, Spisso KR, Natarajan N, Rosenfeld D, Leiman S, Korn D. Successful treatment of fetal congestive heart failure secondary to tachycardia. N Engl J Med. 1981;304:1527–9.

    CAS  PubMed  Google Scholar 

  120. Hatjis CG. Nonimmunologic fetal hydrops associated with hyperreactio luteinalis. Obstet Gynecol. 1985;65:11S–3S.

    CAS  PubMed  Google Scholar 

  121. Healsmith S, Savoia H, Kane SC. How clinically important are non-D Rh antibodies? Acta Obstet Gynecol Scand. 2019;98:877–84.

    CAS  PubMed  Google Scholar 

  122. Hellman LM, Hertig AT. Pathological changes in the placenta associated with erythroblastosis of the fetus. Am J Pathol. 1937;14:111–20.

    Google Scholar 

  123. Hendricks SK, Sorensen TK, Baker ER. Trisomy 21, fetal hydrops, and anemia: prenatal diagnosis of transient myeloproliferative disorder? Obstet Gynecol. 1993;82:703–5.

    CAS  PubMed  Google Scholar 

  124. Hendrickson JE, Delaney M. Hemolytic disease of the fetus and newborn: modern practice and future investigations. Transfus Med Rev. 2016;30:159–64.

    PubMed  Google Scholar 

  125. Hogge WA, Hogge JS, Schnatterly PT, Sun CJ, Blitzer MG. Congenital nephrosis: detection of index cases through maternal serum α-fetoprotein screening. Am J Obstet Gynecol. 1992;167:1330–3.

    CAS  PubMed  Google Scholar 

  126. Houston CS, Brown AB. An unusual complication of intrauterine transfusion. Can Med Assoc J. 1966;94:1274–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Hoyer JR, Michael AF, Good RA, Vernier RL. The nephrotic syndrome of infancy: clinical, morphologic, and immunologic studies of four infants. Pediatrics. 1967;40:233–46.

    CAS  PubMed  Google Scholar 

  128. Hoyer JR, Mauer SM, Kjellstrand CM, Buselmeier TJ, Simmons RL, Michael AF, Najarian JS, Vernier RL. Successful renal transplantation in 3 children with congenital nephrotic syndrome. Lancet. 1973;i:1410–3.

    Google Scholar 

  129. Hung P-L, Huang C-C, Huang T-S. Nephrotic syndrome in a Chinese infant. Am J Dis Child. 1977;131:557–9.

    CAS  PubMed  Google Scholar 

  130. Iakovtsova AG. Morphologic changes in the placenta in isoantigenic incompatibility of maternal and fetal blood. Pediatr Akus Ginekol. 1964;1:53–5.

    Google Scholar 

  131. Imakita M, Yutani C, Ishibashi-Ueda H, Murakami M, Chiba Y. A case of hydrops fetalis due to placental chorangioma. Acta Pathol Jpn. 1988;38:941–5.

    CAS  PubMed  Google Scholar 

  132. Irani D, Kim HS, El-Hibri H, Dutton RV, Beaudet A, Armstrong D. Postmortem observations on β-glucuronidase deficiency presenting as hydrops fetalis. Ann Neurol. 1983;14:486–90.

    CAS  PubMed  Google Scholar 

  133. Isaacs H. Fetal hydrops associated with tumors. Am J Perinatol. 2008;25(1):43–68.

    PubMed  Google Scholar 

  134. Ittiwut C, Natesirinilkul R, Tongprasert F, Sathitsamitphong L, Choed-Amphai C, Fanhchaksai K, Charoenkwan P, Suphapeetiporn K, Shotelersuk V. Novel mutations in SPTA1 and SPTB identified by whole exome sequencing in eight Thai families with hereditary pyropoikilocytosis presenting with severe fetal and neonatal anaemia. Br J Haematol. 2019;185:578–82.

    CAS  PubMed  Google Scholar 

  135. Izquierdo L, Kushnir O, Sanchez D, Curet L, Olney P, Sarto GE, Clericuzio C, Olney R. Prenatal diagnosis of Noonan’s syndrome in a female infant with spontaneous resolution of cystic hygroma and hydrops. West J Med. 1990;152:418–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Jackson MR, Carney EW, Lye SJ, Knox Ritchie JW. Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta. 1994;15:341–53.

    CAS  PubMed  Google Scholar 

  137. Jain V, Clarke G, Russell L, McBrien A, Hornberger L, Young C, Chandra S. A case of alloimmune thrombocytopenia, hemorrhagic anemia-induced fetal hydrops, maternal mirror syndrome, and human chorionic gonadotropin-induced thyrotoxicosis. AJP Rep. 2013;203:41–4.

    Google Scholar 

  138. James GB. Histology of the placenta after repeated intrauterine transfusions. Proc R Soc Med. 1970;63:54.

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Jatavan P, Chattipakorn N, Tongsong T. Fetal hemoglobin Bart's hydrops fetalis: pathophysiology, prenatal diagnosis and possibility of intrauterine treatment. J Matern Fetal Neonatal Med. 2018;31:946–57.

    PubMed  Google Scholar 

  140. Jauniaux E, Maldergem LV, De Munter C, Moscoso G, Gillerot Y. Nonimmune hydrops fetalis associated with genetic abnormalities. Obstet Gynecol. 1990;75:568–72.

    CAS  PubMed  Google Scholar 

  141. Jones CJP, Fox H. An ultrastructural study of the placenta in materno-fetal rhesus incompatibility. Virchows Arch A Pathol Anat Histol. 1978;379:229–41.

    CAS  PubMed  Google Scholar 

  142. Jones DED, Pritchard KI, Gioannini CA, Moore DT, Bradford WD. Hydrops fetalis associated with idiopathic arterial calcification. Obstet Gynecol. 1972;39:435–40.

    CAS  PubMed  Google Scholar 

  143. Jordan JA. Identification of human parvovirus B19 infection in idiopathic nonimmune hydrops fetalis. Am J Obstet Gynecol. 1996;174:37–42.

    CAS  PubMed  Google Scholar 

  144. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in the developing human fetus. Early Hum Dev. 1998;52:235–49.

    CAS  PubMed  Google Scholar 

  145. Kamat BR, Greco MA, Demopoulos RI. Immunocytochemical staining patterns of placentas associated with hydrops fetalis. Int J Gynecol Pathol. 1989;8:246–54.

    CAS  PubMed  Google Scholar 

  146. Kan YW, Allen A, Lowenstein L. Hydrops fetalis with alpha thalassemia. N Engl J Med. 1967;276:18–23.

    CAS  PubMed  Google Scholar 

  147. Kaplan C, Blanc WA, Elias J. Identification of erythrocytes in intervillous thrombi: a study using immunoperoxidase identification of hemoglobins. Hum Pathol. 1982;13:554–7.

    CAS  PubMed  Google Scholar 

  148. Kaplan C, Lane B, Miller F, Baker D, Trunca C. Renal pathology of prenatally diagnosed nephrosis. Pediatr Pathol. 1985;3:271–81.

    CAS  PubMed  Google Scholar 

  149. Kaufmann P, Bruns U, Leiser R, Luckhardt M, Winterhager E. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol (Berl). 1985;173:203–14.

    CAS  PubMed  Google Scholar 

  150. Keller CC, Joosten M, Middeldorp AM, Knapen MF. Fetal anemia caused by the Guadalajara variant of G6PD deficiency. Prenat Diagn. 2015;35:1255–7.

    PubMed  Google Scholar 

  151. Kim YA, Makar RS. Detection of fetomaternal hemorrhage. Am J Hematol. 2012;87:417–23.

    PubMed  Google Scholar 

  152. King AJ, Higgs DR. Potential new approaches to the management of the Hb Bart’s hydrops fetalis syndrome: the most severe form of α-thalassemia. Hematology Am Soc Hematol Educ Program. 2018;2018:353–60.

    PubMed  PubMed Central  Google Scholar 

  153. Klein AM, Holzman IR, Austin EM. Fetal tachycardia before the development of hydrops-attempted cardio-version: a case report. Am J Obstet Gynecol. 1979;134:347–8.

    CAS  PubMed  Google Scholar 

  154. Kline BS. Microscopic observations of the placental barrier in transplacental erythrocytotoxic anemia (erythroblastosis fetalis) and in normal pregnancy. Am J Obstet Gynecol. 1948;56:226–37.

    CAS  PubMed  Google Scholar 

  155. Kleinman CS, Donnerstein RL, Devore GR, Jaffe CC, Lynch DC, Berkowitz RL, Talner NS, Hobbins JC. Fetal echocardiography for evaluation of in utero congestive heart failure. A technique for study of nonimmune hydrops. N Engl J Med. 1982;306:568–75.

    CAS  PubMed  Google Scholar 

  156. Knilans TK. Cardiac abnormalities associated with hydrops fetalis. Semin Perinatol. 1995;19:483–92.

    CAS  PubMed  Google Scholar 

  157. Knisely AS. Placental siderosis in maternal β-thalassemia. Am J Obstet Gynecol. 1990;162:1638–9.

    CAS  PubMed  Google Scholar 

  158. Koffler H, Papile L-A, Burstein R. Congenital chylothorax: two cases associated with maternal polyhydramnios. Am J Dis Child. 1978;132:638.

    CAS  PubMed  Google Scholar 

  159. Kohler HG. Cardiovascular malformation and hydramnios. Obstet Gynecol. 1966;28:473–8.

    CAS  PubMed  Google Scholar 

  160. Kohler HG, Rymer B. Congenital cystic malformation of the lung and its relation to hydramnios. J Obstet Gynaecol Br Commonw. 1973;80:130–4.

    PubMed  Google Scholar 

  161. Krause JR, Penchansky L, Knisely AS. Morphological diagnosis of parvovirus B19 infection. Arch Pathol Lab Med. 1992;116:178–80.

    CAS  PubMed  Google Scholar 

  162. Lacro RV, Jones KL, Benirschke K. Coarctation of the aorta in Turner syndrome: a pathologic study of fetuses with nuchal hygromas, hydrops fetalis, and female genitalia. Pediatrics. 1988;81:445–51.

    CAS  PubMed  Google Scholar 

  163. Lage JM. Placentomegaly with massive hydrops of placental stem villi, diploid DNA content, and omphaloceles: possible association with Beckwith-Wiedemann syndrome. Hum Pathol. 1991;22:591–7.

    CAS  PubMed  Google Scholar 

  164. Lai K, Li S, Lin W, Yang D, Chen W, Li M, Pang L, Chen P. Invasive prenatal diagnosis of α-thalassemia to control Hb Bart's hydrops fetalis syndrome: 15 years of experience. Arch Gynecol Obstet. 2018;298:307–11.

    PubMed  Google Scholar 

  165. Lal A, Goldrich ML, Haines DA, Azimi M, Singer ST, Vichinsky EP. Heterogeneity of hemoglobin H disease in childhood. N Engl J Med. 2011;364:710–8.

    CAS  PubMed  Google Scholar 

  166. Lallemand AV, Doco-Fenzy M, Gaillard DA. Investigation of nonimmune hydrops fetalis: multidisciplinary studies are necessary for diagnosis – review of 94 cases. Pediatr Dev Pathol. 1999;2:432–9.

    CAS  PubMed  Google Scholar 

  167. Lam Y-H, Tang MH-Y, Lee C-P, Tse H-Y. Prenatal ultrasonographic prediction of homozygous type 1 α-thalassemia at 12 to 13 weeks of gestation. Am J Obstet Gynecol. 1999;180:148–50.

    CAS  PubMed  Google Scholar 

  168. Landrum BG, Johnson DE, Ferrara B, Boros SJ, Thompson TR. Hydrops fetalis and chromosomal trisomies. Am J Obstet Gynecol. 1986;154:1114–5.

    CAS  PubMed  Google Scholar 

  169. Langer JC, Harrison MR, Schmidt KG, Silverman NH, Anderson RL, Goldberg JD, Filly RA, Crombleholme TM, Longaker MT, Golbus MS. Fetal hydrops and death from sacrococcygeal teratoma: rationale for fetal surgery. Am J Obstet Gynecol. 1989;160:1145–50.

    CAS  PubMed  Google Scholar 

  170. Laros RK, Kalstone CE. Sickle cell β-thalassemia and pregnancy. Obstet Gynecol. 1971;37:67–71.

    PubMed  Google Scholar 

  171. Leake RD, Strimling B, Emmanouilidis GC. Intrauterine cardiac failure with hydrops fetalis. Case report in a twin with the hypoplastic left heart syndrome and review of the literature. Clin Pediatr. 1973;12:649–51.

    CAS  Google Scholar 

  172. Le Bouar G, Lassel L, Loeuillet-Olivo L, d'Herve D, Poulain P. Le neuroblastome métastatique anténatal: critères pronostiques. A propos d'un cas [Antenatal metastatic neuroblastoma: prognostic criteria. A case report]. J Gynecol Obstet Biol Reprod (Paris). 2003;32:740–4.

    PubMed  Google Scholar 

  173. Lee CH, Lau TK, To KF, Lam HS, Chan AW, Ng PC. Congenital systemic Langerhans cell histiocytosis presenting as hydrops fetalis. Acta Paediatr. 2005;94(12):1843–7. https://doi.org/10.1111/j.1651-2227.2005.tb01866.x. PMID: 16431411.

    Article  PubMed  Google Scholar 

  174. Lewis NE, Marszalek L, Ernst LM. Placental pathologic features in Fetomaternal hemorrhage detected by flow cytometry. Pediatr Dev Pathol. 2017;20:142–51.

    PubMed  Google Scholar 

  175. Léticée N, Bessières-Grattagliano B, Dupré T, Vuillaumier-Barrot S, de Lonlay P, Razavi F, El Khartoufi N, Ville Y, Vekemans M, Bouvier R, Seta N, Attié-Bitach. T. Should PMM2-deficiency (CDG Ia) be searched in every case of unexplained hydrops fetalis? Mol Genet Metab. 2010;101:253–7.

    PubMed  Google Scholar 

  176. Lie-Injo LE. Haemoglobin of new-born infants in Indonesia. Nature. 1959;183:1125–6.

    CAS  Google Scholar 

  177. Lie-Injo LE. Alpha-chain thalassemia and hydrops fetalis in Malaysia; report of 5 cases. Blood. 1962;20:581–90.

    CAS  PubMed  Google Scholar 

  178. Lie-Injo LE, Lopez CG, Dutt AK. Pathological findings in hydrops foetalis due to alpha-thalassemia: a review of 32 cases. Trans R Soc Trop Med Hyg. 1968;62:874–9.

    CAS  PubMed  Google Scholar 

  179. Liu YC, Mai YL, Chang CC, Chen KW, Chow SN. The presence of hydrops fetalis in a fetus with congenital mesoblastic nephroma. Prenat Diagn. 1996;16:363–5.

    CAS  PubMed  Google Scholar 

  180. Liley AW. Intrauterine transfusion of fetus in haemolytic disease. Br Med J. 1963;2:1107–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Lingman G, Lundström NR, Marsal K, Ohrlander S. Fetal cardiac arrhythmia – clinical outcome in 113 cases. Acta Obstet Gynecol Scand. 1986;65:263–7.

    CAS  PubMed  Google Scholar 

  182. Lockwood CJ, Nadel AS, King ME, Roberts DJ. Case 16–2009: a 32-year-old pregnant woman with an abnormal fetal ultrasound study. N Engl J Med. 2009;360:2225–35.

    CAS  PubMed  Google Scholar 

  183. Loh TJ, Lian DW, Iyer P, Lam JC, Kuick CH, Aung AC, Chang KT. Congenital GATA1-mutated myeloproliferative disorder in trisomy 21 complicated by placental fetal thrombotic vasculopathy. Hum Pathol. 2014;45:2364–7.

    CAS  PubMed  Google Scholar 

  184. Long A, Sinkovskaya ES, Edmondson AC, Zackai E, Schrier Vergano SA. Kabuki syndrome as a cause of non-immune fetal hydrops/ascites. Am J Med Genet A. 2016;170:3333–7.

    CAS  PubMed  Google Scholar 

  185. Lord J, McMullan DJ, Eberhardt RY, Rinck G, Hamilton SJ, Quinlan-Jones E, Prigmore E, Keelagher R, Best SK, Carey GK, Mellis R, Robart S, Berry IR, Chandler KE, Cilliers D, Cresswell L, Edwards SL, Gardiner C, Henderson A, Holden ST, Homfray T, Lester T, Lewis RA, Newbury-Ecob R, Prescott K, Quarrell OW, Ramsden SC, Roberts E, Tapon D, Tooley MJ, Vasudevan PC, Weber AP, Wellesley DG, Westwood P, White H, Parker M, Williams D, Jenkins L, Scott RH, Kilby MD, Chitty LS, Hurles ME, Maher ER. Prenatal Assessment of Genomes and Exomes Consortium. Prenatal exome sequencing analysis in fetal structural anomalies detected by ultrasonography (PAGE): a cohort study. Lancet. 2019;393:747–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  186. Lorey F, Charoenkwan P, Witkowska HE, Lafferty J, Patterson M, Eng B, Waye JS, Finklestein JZ, Chui DHK. HbH hydrops foetalis syndrome: a case report and review of literature. Br J Haematol. 2001;115:72–8.

    CAS  PubMed  Google Scholar 

  187. Losure TA, Roberts NS. In utero diagnosis of atrial flutter by means of real-time-direct M-mode echocardiography. Am J Obstet Gynecol. 1984;149:903–5.

    CAS  PubMed  Google Scholar 

  188. Louderback AL, Shanbrom E. Hemoglobin electrophoresis. JAMA. 1967;202:718–9.

    CAS  PubMed  Google Scholar 

  189. Lynn AAA, Parry SI, Morgan MA, Mennuti MT. Disseminated congenital neuroblastoma involving the placenta. Arch Pathol Lab Med. 1997;121:741–4.

    CAS  PubMed  Google Scholar 

  190. Macgregor SN, Socol ML, Pielet BW, Sholl JT, Minogue JP. Prediction of fetoplacental blood volume in isoimmunized pregnancy. Am J Obstet Gynecol. 1988;159:1493–7.

    CAS  PubMed  Google Scholar 

  191. Machin GA. Hydrops revisited: literature review of 1,414 cases published in the 1980s. Am J Med Genet. 1989;34:366–90.

    CAS  PubMed  Google Scholar 

  192. Mahajan P, Margolin J, Iacobas I. Kasabach-Merritt Phenomenon: Classic Presentation and Management Options. Clin Med Insights Blood Disord. 2017;10:1179545X17699849.

    Google Scholar 

  193. Makhamreh MM, Cottingham N, Ferreira CR, Berger S, Al-Kouatly HB. Nonimmune hydrops fetalis and congenital disorders of glycosylation: a systematic literature review. J Inherit Metab Dis. 2020;43:223–33.

    PubMed  Google Scholar 

  194. Manning FA, Heaman M, Boyce D, Carter LJ. Intrauterine fetal tachypnea. Obstet Gynecol. 1981;58:398–400.

    CAS  PubMed  Google Scholar 

  195. Mardy AH, Chetty SP, Norton ME, Sparks TN. A system-based approach to the genetic etiologies of non-immune hydrops fetalis. Prenat Diagn. 2019;39:732–50.

    PubMed  PubMed Central  Google Scholar 

  196. Mark K, Reis A, Zenker M. Prenatal findings in four consecutive pregnancies with fetal Pierson syndrome, a newly defined congenital nephrosis syndrome. Prenat Diagn. 2006;26:262–6.

    PubMed  Google Scholar 

  197. Martin-Almedina S, Mansour S, Ostergaard P. Human phenotypes caused by PIEZO1 mutations; one gene, two overlapping phenotypes? J Physiol. 2018;596:985–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  198. Martinez AE, Robinson MJ, Alexis JB. Kaposiform hemangioendothelioma associated with nonimmune fetal hydrops. Arch Pathol Lab Med. 2004;128:678–81.

    PubMed  Google Scholar 

  199. Matalon ST, Blank M, Ornoy A, Shoenfeld Y. The association between anti-thyroid antibodies and pregnancy loss. Am J Reprod Immunol. 2001;45:72–7.

    CAS  PubMed  Google Scholar 

  200. McCarthy WA, Popek EJ. Persistence of villous immaturity in term deliveries following intrauterine transfusion for parvovirus B19 infection and RhD-associated hemolytic disease of the fetus and newborn. Pediatr Dev Pathol. 2017;20:469–74.

    PubMed  Google Scholar 

  201. McFadden DE, Taylor GP. Cardiac abnormalities and nonimmune hydrops fetalis: a coincidental, not causal, relationship. Pediatr Pathol. 1989;9:11–7.

    CAS  PubMed  Google Scholar 

  202. McPherson E. Hydrops fetalis in a cohort of 3,137 stillbirths and second trimester miscarriages. Am J Med Genet A. 2019;179:2338–42.

    CAS  PubMed  Google Scholar 

  203. Meizner I, Levy A, Carmi R, Robinsin C. Niemann-Pick disease associated with nonimmune hydrops fetalis. Am J Obstet Gynecol. 1990;163:128–9.

    CAS  PubMed  Google Scholar 

  204. Mentzer WC, Collier E. Hydrops fetalis associated with erythrocyte G-6-PD deficiency and maternal ingestion of fava beans and ascorbic acid. J Pediatr. 1975;86:565–7.

    CAS  PubMed  Google Scholar 

  205. Meznarich JA, Draper L, Christensen RD, Yaish HM, Luem ND, Pysher TJ, Jung G, Nemeth E, Ganz T, Ward DM. Fetal presentation of congenital dyserythropoietic anemia type 1 with novel compound heterozygous CDAN1 mutations. Blood Cells Mol Dis. 2018;71:63–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  206. Miller DF, Petrie SJ. Fatal erythroblastosis fetalis secondary to AB0 incompatibility. Obstet Gynecol. 1963;22:773–7.

    CAS  PubMed  Google Scholar 

  207. Miller PD, Smith BC, Marinoff DN. Theca-lutein ovarian cysts associated with homozygous α-thalassemia. Am J Obstet Gynecol. 1987;157:912–4.

    CAS  PubMed  Google Scholar 

  208. Mills AE, Emms M, Licata SG. A simple technique for preparation of bone marrow or peripheral blood buffy coat cells for electron microscopy. Ultrastruct Pathol. 1990;14:173–6.

    CAS  PubMed  Google Scholar 

  209. Milunsky A, Alpert E, Frigoletto FD, Driscoll SG, McCluskey RT, Colvin RB. Prenatal diagnosis of the congenital nephrotic syndrome. Pediatrics. 1977;59:770–3.

    CAS  PubMed  Google Scholar 

  210. Minagawa Y, Akaiwa A, Hidaka T, Tsuzaki T, Tatsumura M, Ito T, Maeda K. Severe fetal supraventricular bradyarrhythmia without fetal hypoxia. Obstet Gynecol. 1987;70:454–6.

    CAS  PubMed  Google Scholar 

  211. Mittendorf R, Williams MA. RHo(D) immunoglobulin (RhoGAM): how it came into being. Obstet Gynecol. 1991;77:301–3.

    CAS  PubMed  Google Scholar 

  212. Mogilner BM, Ashkenazy M, Borenstein R, Lancet M. Hydrops fetalis caused by maternal indomethacin treatment. Acta Obstet Gynecol Scand. 1982;61:183–5.

    CAS  PubMed  Google Scholar 

  213. Moise KJ Jr. Non-anti-D antibodies in red-cell alloimmunization. Eur J Obstet Gynecol Reprod Biol. 2000;92:75–81.

    CAS  PubMed  Google Scholar 

  214. Moise KJ Jr. Fetal RhD typing with free DNA in maternal plasma. Am J Obstet Gynecol. 2005;192:663–5.

    PubMed  Google Scholar 

  215. Moller JH, Lynch RP, Edwards JE. Fetal cardiac failure resulting from congenital anomalies of the heart. J Pediatr. 1966;68:699–703.

    CAS  PubMed  Google Scholar 

  216. Mor Z, Schreyer P, Wainraub Z, Hayman E, Caspi E. Nonimmune hydrops fetalis associated with angioosteohypertrophy (Klippel-Trenaunay) syndrome. Am J Obstet Gynecol. 1988;159:1185–6.

    CAS  PubMed  Google Scholar 

  217. Moreno CA, Kanazawa T, Barini R, Nomura ML, Andrade KC, Gomes CP, Heinrich JK, Giugliani R, Burin M, Cavalcanti DP. Non-immune hydrops fetalis: a prospective study of 53 cases. Am J Med Genet A. 2013;161A:3078–86.

    PubMed  Google Scholar 

  218. Moss TJ, Kaplan L. Association of hydrops fetalis with congenital neuroblastoma. Am J Obstet Gynecol. 1978;132:905–6.

    CAS  PubMed  Google Scholar 

  219. Mostoufi-Zadeh M, Weiss LM, Driscoll SG. Nonimmune hydrops fetalis: a challenge in perinatal pathology. Hum Pathol. 1985;16:785–9.

    CAS  PubMed  Google Scholar 

  220. Moya FR, Grannum PAT, Widness JA, Clemons GK, Copel JA, Hobbins JC. Erythropoietin in human fetuses with immune hemolytic anemia and hydrops fetalis. Obstet Gynecol. 1993;82:353–8.

    CAS  PubMed  Google Scholar 

  221. Naeye RL. New observations in erythroblastosis fetalis. JAMA. 1967;200:105–10.

    Google Scholar 

  222. Najafipour F, Aliasgarzadeh A, Aghamohamadzadeh N, Bahrami A, Mobasri M, Niafar M, Khoshbaten M. A cross-sectional study of metabolic and endocrine complications in beta-thalassemia major. Ann Saudi Med. 2008;28:361–6.

    PubMed  PubMed Central  Google Scholar 

  223. Nakamura Y, Komatsu Y, Yano H, Kitazono S, Hosokawa Y, Fukuda S, Kawano S, Nagasue N, Matsunaga T, Aiko Y, Hashimoto T, Morimatsu M. Nonimmunologic hydrops fetalis: a clinicopathological study of 50 autopsy cases. Pediatr Pathol. 1987;7:19–30.

    CAS  PubMed  Google Scholar 

  224. Nakayama R, Yamada D, Steinmiller V, Hsia E, Hale RW. Hydrops fetalis secondary to Bart hemoglobinopathy. Obstet Gynecol. 1986;67:176–80.

    CAS  PubMed  Google Scholar 

  225. Nassr AA, Ness A, Hosseinzadeh P, Salmanian B, Espinoza J, Berger V, Werner E, Erfani H, Welty S, Bateni ZH, Shamshirsaz AA, Popek E, Ruano R, Davis AS, Lee TC, Keswani S, Cass DL, Olutoye OO, Belfort MA, Shamshirsaz AA. Outcome and treatment of antenatally diagnosed nonimmune hydrops fetalis. Fetal Diagn Ther. 2018;43:123–8.

    PubMed  Google Scholar 

  226. Nathan DG. Thalassemia. N Engl J Med. 1972;286:586–97.

    CAS  PubMed  Google Scholar 

  227. Nathan DG. Thalassemia: a progress report on applied molecular biology. N Engl J Med. 1973;288:1122–3.

    CAS  PubMed  Google Scholar 

  228. Nelson A, Peterson LA, Frampton B, Sly WS. Mucopolysaccharidosis VII (β-glucuronidase deficiency) presenting as nonimmune hydrops fetalis. J Pediatr. 1982;101:574–6.

    CAS  PubMed  Google Scholar 

  229. Newton ER, Louis F, Dalton ME, Feingold M. Fetal neuroblastoma and catecholamine-induced maternal hypertension. Obstet Gynecol. 1985;65:49S–52S.

    CAS  PubMed  Google Scholar 

  230. Nicolaides KH, Soothill PW, Clewell WH, Rodeck CH, Mibashan RS, Campbell S. Fetal haemoglobin measurement of red cell isoimmunization. Lancet. 1988;i:1073–5.

    Google Scholar 

  231. Nicolaides KH, Thilaganathan B, Rodeck CH, Mibashan RS. Erythroblastosis and reticulocytosis in anemic fetuses. Am J Obstet Gynecol. 1988;159:1063–5.

    CAS  PubMed  Google Scholar 

  232. Nicolaides KH, Thilaganathan B, Mibashan RS. Cordocentesis in the investigation of fetal erythropoiesis. Am J Obstet Gynecol. 1989;161:1197–200.

    CAS  PubMed  Google Scholar 

  233. Nimrod C, Davies D, Harder J, Iwanicki S, Kondo C, Takahashi Y, Maloney J, Persaud D, Nicholson S. Ultrasound evaluation of tachycardia-induced hydrops in the fetal lamb. Am J Obstet Gynecol. 1987;157:655–9.

    CAS  PubMed  Google Scholar 

  234. Nitta H, Taira Y, Kinjo T, Chinen Y, Masamoto H, Sanabe N, Goya H, Yoshida T, Sugibayashi R, Sumie M, Wada S, Sago H, Aoki Y. Fetal thoracoamniotic shunting in a case of congenital pulmonary airway malformations with hydrops fetalis. AJP Rep. 2017;7:e185–7.

    PubMed  PubMed Central  Google Scholar 

  235. Nogami W, Weber T, Lemons JA. Hydrops fetalis associated with midgut volvulus. J Pediatr Surg. 1985;20:177–8.

    CAS  PubMed  Google Scholar 

  236. Ohyama M, Kobayashi S, Aida N, Toyoda Y, Ijiri R, Tanaka Y. Congenital neuroblastoma diagnosed by placental examination. Med Pediatr Oncol. 1999;33:430–1.

    CAS  PubMed  Google Scholar 

  237. Olson RW, Nishibatake M, Arya S, Gilbert EF. Nonimmunologic hydrops fetalis due to intrauterine closure of fetal foramen ovale. In: Gilbert EF, editor. Genetic aspects of developmental pathology, vol 23(1), Birth defects: original article series. New York: Alan R. Liss; 1987. p. 433–42.

    Google Scholar 

  238. Orkin SH, Nathan DG. Current concepts in genetics. N Engl J Med. 1976;295:710–4.

    CAS  PubMed  Google Scholar 

  239. Östör AG, Fortune DW. Tuberous sclerosis initially seen as hydrops fetalis. Report of a case and review of the literature. Arch Pathol Lab Med. 1978;102:34–9.

    PubMed  Google Scholar 

  240. Oudesluys-Murphy AM. Nonimmune hydrops fetalis in Noonan’s syndrome. Am J Dis Child. 1987;141:478–9.

    CAS  PubMed  Google Scholar 

  241. Özmen S, Seçkin N, Turhan NÖ, Dilmen G, Dilmen U. Fetal methemoglobinemia: a cause of nonimmune hydrops. Am J Obstet Gynecol. 1995;173:232–3.

    PubMed  Google Scholar 

  242. Pattison N, Roberts A. The management of severe erythroblastosis fetalis by fetal transfusion: survival of transfused adult erythrocytes in the fetus. Obstet Gynecol. 1989;74:901–4.

    CAS  PubMed  Google Scholar 

  243. Pearson HA, Shanklin DR, Brodine CR. Alpha-thalassemia as cause of nonimmunological hydrops. Am J Dis Child. 1965;109:168–72.

    CAS  PubMed  Google Scholar 

  244. Peng HH, Wang TH, Chao AS, Chang YL, Shieh SC, Chang SD. Klippel-Trenaunay-Weber syndrome involving fetal thigh: prenatal presentations and outcomes. Prenat Diagn. 2006;26:825–30.

    PubMed  Google Scholar 

  245. Peng HQ, Levitin-Smith M, Rochelson B, Kahn E. Umbilical cord stricture and overcoiling are common causes of fetal demise. Pediatr Dev Pathol. 2006;9:14–9.

    PubMed  Google Scholar 

  246. Perkins RP. Hydrops fetalis and stillbirth in a male glucose-6-phosphate dehydrogenase-deficient fetus possibly due to maternal ingestion of sulfisoxazole. Am J Obstet Gynecol. 1971;111:379–81.

    CAS  PubMed  Google Scholar 

  247. Perkins DG, Kopp CM, Haust MD. Placental infiltration in congenital neuroblastoma: a case study with ultrastructure. Histopathology. 1980;4:383–9.

    CAS  PubMed  Google Scholar 

  248. Peterson JA, McFarland JG, Curtis BR, Aster RH. Neonatal alloimmune thrombocytopenia: pathogenesis, diagnosis and management. Br J Haematol. 2013;161:3–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  249. Pielet BW, Socol ML, Macgregor SN, Ney JA, Dooley SL. Cordocentesis: an appraisal of risks. Am J Obstet Gynecol. 1988;159:1497–500.

    CAS  PubMed  Google Scholar 

  250. Pilz I, Schweikhart G, Kaufmann P. Zur Abgrenzung normaler, artefizieller und pathologischer Strukturen in reifen menschlichen Plazentarzotten. III. Morphometrische Untersuchungen bei Rhesus-Inkompabilität. Arch Gynecol. 1980;229:137–54.

    CAS  PubMed  Google Scholar 

  251. Poissonnier MH, Brossard Y, Demedeiros N, Vassileva J, Parnet F, Larsen M, Gosset M, Chavinie J, Huchet J. Two hundred intrauterine exchange transfusions in severe blood incompatibilities. Am J Obstet Gynecol. 1989;161:709–13.

    CAS  PubMed  Google Scholar 

  252. Pootrakul S, Wasi P, Na-Nakorn S. Haemoglobin Bart’s hydrops foetalis in Thailand. Ann Hum Genet. 1967;30:293–311.

    CAS  PubMed  Google Scholar 

  253. Potter EL. Universal edema of the fetus unassociated with erythroblastosis. Am J Obstet Gynecol. 1943;46:130–4.

    Google Scholar 

  254. Queenan JT, Douglas GR. Intrauterine transfusion: a preliminary report. Obstet Gynecol. 1965;25:308–21.

    CAS  PubMed  Google Scholar 

  255. Rabinowitz P, Harris EJ, Friedman IS. Theca-lutein cysts of the ovaries. A case of erythroblastosis with abruptio placentae and acute renal failure. JAMA. 1961;177:509–10.

    CAS  PubMed  Google Scholar 

  256. Radunovic N, Lockwood CJ, Alvarez M, Plecas D, Chitkara U, Berkovitz RL. The severely anemic and hydropic isoimmune fetus: changes in fetal hematocrit associated with intrauterine death. Obstet Gynecol. 1992;79:390–3.

    CAS  PubMed  Google Scholar 

  257. Ranucci-Weiss D, Uerpairojkit B, Bowles N, Towbin JA, Chan L. Intrauterine adenoviral infection associated with fetal non-immune hydrops. Prenat Diagn. 1998;18:182–5.

    CAS  PubMed  Google Scholar 

  258. Ravindranath Y, Paglia DE, Warrier I, Valentine W, Nakatani M, Brockway RA. Glucose phosphate isomerase deficiency as a cause of hydrops fetalis. N Engl J Med. 1987;316:258–61.

    CAS  PubMed  Google Scholar 

  259. Ravishankar S, Migliori A, Struminsky J, Has P, Sung CJ, He M. Placental findings in feto-maternal hemorrhage in livebirth and stillbirth. Pathol Res Pract. 2017;213:301–4.

    PubMed  Google Scholar 

  260. Reichert SL, McKay EM, Moldenhauer JS. Identification of a novel nonsense mutation in the FOXP3 gene in a fetus with hydrops—expanding the phenotype of IPEX syndrome. Am J Med Genet Part A. 2016;170A:226–32.

    PubMed  Google Scholar 

  261. Rice GE, Mostoufi-Zadeh M, Kolodny EH, Driscoll SG. Hydrops fetalis in Gaucher’s disease. Teratology. 1984;29:53A–4A.

    Google Scholar 

  262. Roberts DJ, Nadel A, Lage J, Rutherford CJ. An unusual variant of congenital dyserythropoietic anaemia with mild maternal and lethal fetal disease. Br J Haematol. 1993;84:549–51.

    CAS  PubMed  Google Scholar 

  263. Rodeck CH, Nicolaides KH, Warsof SL, Fysh WJ, Gamsu HR, Kemp JR. The management of severe rhesus isoimmunization by fetoscopic intravascular transfusions. Am J Obstet Gynecol. 1984;150:769–74.

    CAS  PubMed  Google Scholar 

  264. Rodin AE, Nichols MM. Congestive heart failure in the fetus and during the first day of life. Tex Med. 1975;72:44–8.

    Google Scholar 

  265. Rodriguez MM, Chaves F, Romaguera RL, Ferrer PL, de la Guardia C, Bruce JH. Value of autopsy in nonimmune hydrops fetalis: series of 51 stillborn fetuses. Pediatr Dev Pathol. 2002;5:365–74.

    PubMed  Google Scholar 

  266. Rogers BB. Histopathologic variability of finding erythroid inclusions with intranuclear parvovirus B19 infection. Pediatr Pathol. 1992;12:883–9.

    CAS  PubMed  Google Scholar 

  267. Rogers BB, Mark Y, Oyer CE. Diagnosis and incidence of fetal parvovirus infection in an autopsy series: I. Histology. Pediatr Pathol. 1993;13:371–9.

    CAS  PubMed  Google Scholar 

  268. Rogers BB, Bloom SL, Buchanan GR. Autosomal dominantly inherited Diamond-Blackfan anemia resulting in nonimmune hydrops. Obstet Gynecol. 1997;89:805–7.

    CAS  PubMed  Google Scholar 

  269. Rönisch P, Kleihauer E. Alpha-Thalassämie mit HbH und Bart’s in einer deutschen Familie. Klin Wchschr. 1967;45:1193–200.

    Google Scholar 

  270. Rund D, Rachmilewitz E. β-thalassemia. N Engl J Med. 2005;353:1135–46.

    CAS  PubMed  Google Scholar 

  271. Rychik J, Khalek N, Gaynor JW, Johnson MP, Adzick NS, Flake AW, Hedrick HL. Fetal intrapericardial teratoma: natural history and management including successful in utero surgery. Am J Obstet Gynecol. 2016;215:780.e1–7.

    PubMed  Google Scholar 

  272. Sacks LM, Polin JI, Breckenridge J. Congenital chylothorax presenting as hydrops fetalis. A case report. J Reprod Med. 1983;28:341–4.

    CAS  PubMed  Google Scholar 

  273. Saltzman DH, Frigoletto FD, Harlow BL, Barss VA, Benacerraf BR. Sonographic evaluation of hydrops fetalis. Obstet Gynecol. 1989;74:106–11.

    CAS  PubMed  Google Scholar 

  274. Scheffer PG, van der Schoot CE, Page-Christiaens GC, de Haas M. Noninvasive fetal blood group genotyping of rhesus D, c, E and of K in alloimmunised pregnant women: evaluation of a 7-year clinical experience. BJOG. 2011;118:1340–8.

    CAS  PubMed  Google Scholar 

  275. Scheib JS, Waxman J. Congenital heart block in successive pregnancies: a case report and evaluation of risk with therapeutic consideration. Obstet Gynecol. 1989;73:481–4.

    CAS  PubMed  Google Scholar 

  276. Schumacher B, Moise KJ. Fetal transfusion for red blood cell alloimmunization. In pregnancy. Obstet Gynecol. 1996;88:137–50.

    CAS  PubMed  Google Scholar 

  277. Schwab M, Niemeyer C, Schwarzer U. Down syndrome, transient myeloproliferative disorder, and infantile liver fibrosis. Med Pediatr Oncol. 1998;31:159–65.

    CAS  PubMed  Google Scholar 

  278. Schwanitz G, Zerris K, Niesen M, Haverkamp F, Schmid G. Hydrops fetalis as an indication for prenatal chromosome analysis with the example of the diagnosis of a duplication 15q11 and 17q25 due to familial translocation 15/17. Ann Genet. 1988;31:186–9.

    CAS  PubMed  Google Scholar 

  279. Schwartz SM, Visekul C, Laxova R, McPherson E, Gilbert EF. Idiopathic hydrops fetalis report of 4 patients including 2 affected sibs. Am J Med Genet. 1981;8:59–66.

    CAS  PubMed  Google Scholar 

  280. Seeds JW, Bowes WA, Chescheir NC. Echogenic venous turbulence is a critical feature of successful intravascular transfusion. Obstet Gynecol. 1989;73:488–90.

    CAS  PubMed  Google Scholar 

  281. Seifer DB, Ferguson JE, Behrens CM, Zemel S, Stevenson DK, Ross J. Nonimmune hydrops fetalis in association with hemangioma of the umbilical cord. Obstet Gynecol. 1985;66:283–6.

    CAS  PubMed  Google Scholar 

  282. Seppälä M, Aula P, Rapola J, Karjalainen O, Huttunen N-P, Ruoslahti E. Congenital nephrotic syndrome: prenatal diagnosis and genetic counselling by estimation of amniotic-fluid and maternal serum alpha-fetoprotein. Lancet. 1976;i:123–5.

    Google Scholar 

  283. Seward JF, Zusman J. Hydrops fetalis associated with small-bowel volvulus. Lancet. 1978;ii:52–3.

    Google Scholar 

  284. Shahin B, Papadopoulou ZL, Jenis EH. Congenital nephrotic syndrome associated with congenital toxoplasmosis. J Pediatr. 1974;85:366–70.

    CAS  PubMed  Google Scholar 

  285. Shimokawa H, Hara K, Fukuda A, Nakano H. Idiopathic hydrops fetalis successfully treated in utero. Obstet Gynecol. 1988;71:984–6.

    CAS  PubMed  Google Scholar 

  286. Shiraishi S, Kinukawa N, Nakano H, Sueishi K. Immunohistochemical distribution of vascular endothelial growth factor in the human placenta associated with hydrops fetalis. Pediatr Pathol Lab Med. 1997;17:65–81.

    CAS  PubMed  Google Scholar 

  287. Silber DL, Durnim RE. Intrauterine atrial tachycardia. Associated with massive edema in a newborn. Am J Dis Child. 1969;117:722–6.

    CAS  PubMed  Google Scholar 

  288. Silver MM, Beverley DW, Valberg LS, Cutz E, Phillips MJ, Shaheed WA. Perinatal hemochromatosis. Clinical, morphologic, and quantitative iron studies. Am J Pathol. 1989;128:538–54.

    Google Scholar 

  289. Silverstein AJ, Kanbour AI. Repetitive idiopathic fetal hydrops. Obstet Gynecol. 1981;57:18S–21S.

    CAS  PubMed  Google Scholar 

  290. Singhal PK, Singh M, Paul VK, Deorari AK, Ghorpade MG. Spectrum of neonatal hyperbilirubinemia: an analysis of 454 cases. Indian Pediatr. 1992;29:319–25.

    CAS  PubMed  Google Scholar 

  291. Sklansky M, Greenberg M, Lucas V, Gruslin-Giroux A. Intrapericardial teratoma in a twin fetus: diagnosis and management. Obstet Gynecol. 1997;89:807–9.

    CAS  PubMed  Google Scholar 

  292. Skopec LL, Lakatua DJ. Non-immune fetal hydrops with hepatic hemangioendothelioma and Kasabach-Merritt syndrome: a case report. Pediatr Pathol. 1989;9:87–93.

    CAS  PubMed  Google Scholar 

  293. Smith CR, Chan HSL, DeSa DJ. Placental involvement in congenital neuroblastoma. J Clin Pathol. 1981;34:785–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  294. Smrcek JM, Baschat AA, Germer U, Gloeckner-Hofmann K, Gembruch U. Fetal hydrops and hepatosplenomegaly in the second half of pregnancy: a sign of myeloproliferative disorder in fetuses with trisomy 21. Ultrasound Obstet Gynecol. 2001;17:403–9.

    CAS  PubMed  Google Scholar 

  295. Society for Maternal-Fetal Medicine (SMFM), Norton ME, Chauhan SP, Dashe JS. Society for maternal-fetal medicine (SMFM) clinical guideline #7: nonimmune hydrops fetalis. Am J Obstet Gynecol. 2015;212:127–39.

    Google Scholar 

  296. Society for Maternal-Fetal Medicine (SMFM), Mari G, Norton ME, Stone J, Berghella V, Sciscione AC, Tate D, Schenone MH. Society for Maternal-Fetal Medicine (SMFM) Clinical Guideline #8: the fetus at risk for anemia--diagnosis and management. Am J Obstet Gynecol. 2015;212:697–710.

    Google Scholar 

  297. Socol ML, Macgregor SN, Pielet BW, Tamura RK, Sabbagha RE. Percutaneous umbilical transfusion in severe rhesus isoimmunization: resolution of fetal hydrops. Am J Obstet Gynecol. 1987;157:1369–75.

    CAS  PubMed  Google Scholar 

  298. Songdej D, Babbs C, Higgs DR. BHFS International Consortium. An international registry of survivors with Hb Bart’s hydrops fetalis syndrome. Blood. 2017;129:1251–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  299. Soothill P. Intrauterine blood transfusion for non-immune hydrops fetalis due to parvovirus B19 infection. Lancet. 1990;336:121–2.

    CAS  PubMed  Google Scholar 

  300. Sparks TN, Thao K, Lianoglou BR, Boe NM, Bruce KG, Datkhaeva I, Field NT, Fratto VM, Jolley J, Laurent LC, Mardy AH, Murphy AM, Ngan E, Rangwala N, Rottkamp CAM, Wilson L, Wu E, Uy CC, Valdez Lopez P, Norton ME. University of California Fetal–Maternal Consortium (UCfC). Nonimmune hydrops fetalis: identifying the underlying genetic etiology. Genet Med. 2019;21:1339–44.

    PubMed  Google Scholar 

  301. Stagnaro-Green A. Thyroid autoimmunity and the risk of miscarriage. Best Pract Res Clin Endocrinol Metab. 2004;18:167–81.

    CAS  PubMed  Google Scholar 

  302. Steinke J, Gries FA, Driscoll SG. In vitro studies of insulin inactivation with reference to erythroblastosis fetalis. Blood. 1967;30:359–63.

    CAS  PubMed  Google Scholar 

  303. Stevens DC, Hilliard JK, Schreiner RL, Hurwitz RA, Murrell R, Mirkin LD, Bonderman PW, Nolen PA. Supraventricular tachycardia with edema, ascites, and hydrops in fetal sheep. Am J Obstet Gynecol. 1982;142:316–22.

    CAS  PubMed  Google Scholar 

  304. Strauss L, Driscoll SG. Congenital neuroblastoma involving the placenta. Reports of two cases. Pediatrics. 1964;34:23–31.

    CAS  PubMed  Google Scholar 

  305. Stroustrup A, Plafkin C, Tran TA, Savitz DA. Demographic and behavioral predictors of severe fetomaternal hemorrhage: a case-control study. Neonatology. 2016;109:248–54.

    PubMed  Google Scholar 

  306. Stroustrup A, Trasande LD. Demographics, clinical characteristics and outcomes of neonates diagnosed with fetomaternal haemorrhage. Arch Dis Child Fetal Neonatal Ed. 2012;97:F405–10.

    PubMed  Google Scholar 

  307. Sudrié-Arnaud B, Marguet F, Patrier S, Martinovic J, Louillet F, Broux F, Charbonnier F, Dranguet H, Coutant S, Vezain M, Lanos R, Tebani A, Fuller M, Lamari F, Chambon P, Brehin AC, Trestard L, Tournier I, Marret S, Verspyck E, Laquerrière A, Bekri S. Metabolic causes of nonimmune hydrops fetalis: a next-generation sequencing panel as a first-line investigation. Clin Chim Acta. 2018;481:1–8.

    PubMed  Google Scholar 

  308. Suh YK. α-thalassemia – differential diagnosis. J Perinatol. 1994;14:319–21.

    CAS  PubMed  Google Scholar 

  309. Taweevisit M, Thorner PS. Peripheral villous stromal hyperplasia: a distinctive placental lesion in hemoglobin bart hydrops fetalis. Pediatr Dev Pathol. 2012;15:345–51.

    PubMed  Google Scholar 

  310. Taylor PV, Scott JS, Gerbis LM, Esscher E, Scott O. Maternal antibodies against fetal cardiac antigens in congenital complete heart block. N Engl J Med. 1986;315:667–72.

    CAS  PubMed  Google Scholar 

  311. Taylor MY, Wyatt-Ashmead J, Gray J, Bofill JA, Martin R, Morrison JC. Pregnancy loss after first-trimester viability in women with sickle trait: time for a reappraisal? Am J Obstet Gynecol. 2006;194:1604–8.

    PubMed  Google Scholar 

  312. Tekinalp G, Sarici SU, Erdinç AS, Gögüş S, Balci S, Gürgey A. Lethal hydrops fetalis due to congenital dyserythropoietic anemia in a newborn: association of a new skeletal abnormality. Pediatr Hematol Oncol. 2001;18:537–42.

    CAS  PubMed  Google Scholar 

  313. Terry J, Pluchinotta FR, Sanders SP, Vergilio JA, Hyde SR, Boyd TK. Congenital langerhans cell histiocytosis with placental involvement. Pediatr Dev Pathol. 2013;16:224–8.

    PubMed  Google Scholar 

  314. Thilaganathan B, Salvesen DR, Abbas A, Ireland RM, Nicolaides KH. Fetal plasma erythropoietin concentration in red blood cellisoimmunized pregnancies. Am J Obstet Gynecol. 1992;167:1292–7.

    CAS  PubMed  Google Scholar 

  315. Thumasathit B, Nondasuta A, Silpisornkosol S, Lousuebsakul B, Unchalipongse P, Mangkornkanok M. Hydrops fetalis associated with Bart’s hemoglobin in northern Thailand. J Pediatr. 1968;73:132–8.

    CAS  PubMed  Google Scholar 

  316. Towbin JA, Griffin LD, Martin AB, Nelson S, Siu B, Ayres NA, Demmler G, Moise KJ Jr, Zhang YH. Intrauterine adenoviral myocarditis presenting as nonimmune hydrops fetalis: diagnosis by polymerase chain reaction. Pediatr Infect Dis J. 1994;13:144–50.

    CAS  PubMed  Google Scholar 

  317. Treadwell MC, Sherer DM, Sacks AJ, Ghezzi F, Romero R. Successful treatment of recurrent non-immune hydrops secondary to fetal hyperthyroidism. Obstet Gynecol. 1996;87:838–40.

    CAS  PubMed  Google Scholar 

  318. Tritipsombut J, Sanchaisuriya K, Fucharoen S, Fucharoen G, Siriratmanawong N, Pinmuang-ngam C, Sanchaisuya P. Hemoglobin profiles and hematologic features of thalassemic newborns. Application to screening of α-Thalassemia 1 and hemoglobin E. Arch Pathol Lab Med. 2008;32:1739–45.

    Google Scholar 

  319. Turski DM, Shahidi N, Visekul C, Gilbert E. Nonimmunologic hydrops fetalis. Am J Obstet Gynecol. 1978;131:586–7.

    CAS  PubMed  Google Scholar 

  320. Tynan JA, Angkachatchai AV, Ehrich M, Paladino T, van den Boom D, Oeth P. Multiplexed analysis of circulating cell-free fetal nucleic acids noninvasive prenatal diagnostic RHD testing. Am J Obstet Gynecol. 2011;204(3):251–3. https://doi.org/10.1016/j.ajog.2010.09.028.

    Article  CAS  Google Scholar 

  321. Uno Y, Taniguchi A, Tanaka E. Histochemical studies in Wolman’s disease – report of an autopsy case accompanied with a large amount of milky ascites. Acta Pathol Jpn. 1973;23:779–90.

    CAS  PubMed  Google Scholar 

  322. Vadeyar S, Ramsay M, James D, O'Neill D. Prenatal diagnosis of congenital Wilms' tumor (nephroblastoma) presenting as fetal hydrops. Ultrasound Obstet Gynecol. 2000;16:80–3.

    CAS  PubMed  Google Scholar 

  323. Van den Veyer IB, Moise KJ. Fetal RhD typing by polymerase chain reaction in pregnancies complicated by rhesus alloimmunization. Obstet Gynecol. 1996;88:1061–7.

    Google Scholar 

  324. Van den Veyer IB, Subramanian SB, Hudson KM, Werch J, Moise KJ, Hughes MR. Prenatal diagnosis of the RhD fetal blood type on amniotic fluid by polymerase chain reaction. Obstet Gynecol. 1996;87:419–22.

    Google Scholar 

  325. Van der Slikke JW, Balk AG. Hydramnios with hydrops fetalis and disseminated fetal neuroblastoma. Obstet Gynecol. 1980;55:250–3.

    PubMed  Google Scholar 

  326. Van Kamp IL, Klumper FJCM, Oepkes D, Meerman RH, Scherjon SA, Vandenbussche FPHA, Kanhai HHH. Complications of intrauterine intravascular transfusion for fetal anemia due to re-cell alloimmunization. Am J Obstet Gynecol. 2005;192:171–7.

    PubMed  Google Scholar 

  327. Vaughan JI, Manning M, Warwick RM, Letsky EA, Murray NA, Roberts IAG. Inhibition of erythroid progenitor cells by anti-Kell antibodies in fetal alloimmune anemia. N Engl J Med. 1998;338:798–803.

    CAS  PubMed  Google Scholar 

  328. Veille JC, Sunderland C, Bennett RM. Complete heart block in a fetus associated with maternal Sjögren’s syndrome. Am J Obstet Gynecol. 1985;151:660–1.

    CAS  PubMed  Google Scholar 

  329. Vermeulen MJ, de Haas V, Mulder MF, Flohil C, Fetter WP, van de Kamp JM. Hydrops fetalis and early neonatal multiple organ failure in familial hemophagocytic lymphohistiocytosis. Eur J Med Genet. 2009;52:417–20.

    PubMed  Google Scholar 

  330. Vetter VL, Rashkind WJ. Congenital complete heart block and connective-tissue disease. N Engl J Med. 1983;309:236–8.

    CAS  PubMed  Google Scholar 

  331. Vintzileos AM, Campbell WA, Soberman SM, Nochimson DJ. Fetal atrial flutter and X-linked dominant vitamin D-resistant rickets. Obstet Gynecol. 1985;65:39S–44S.

    CAS  PubMed  Google Scholar 

  332. Wang JJ, Mao JH. The etiology of congenital nephrotic syndrome: current status and challenges. World J Pediatr. 2016;12:149–58.

    PubMed  Google Scholar 

  333. Watson J, Campbell S. Antenatal evaluation and management in nonimmune hydrops fetalis. Obstet Gynecol. 1986;67:589–93.

    CAS  PubMed  Google Scholar 

  334. Watson WJ, Fiegen MM. Fetal thyrotoxicosis associated with nonimmune hydrops. Am J Obstet Gynecol. 1995;172:1039–40.

    CAS  PubMed  Google Scholar 

  335. Weiner CP, Thompson IB. Direct treatment of fetal supraventricular tachycardia after failed transplacental therapy. Am J Obstet Gynecol. 1988;158:570–3.

    CAS  PubMed  Google Scholar 

  336. Weiner C, Varner M, Pringle K, Hein H, Williamson R, Smith WL. Antenatal diagnosis and palliative treatment of nonimmune hydrops fetalis secondary to extralobar sequestration. Obstet Gynecol. 1986;68:275–80.

    CAS  PubMed  Google Scholar 

  337. Weiner CP, Sipes SL, Wenstrom K. The effect of fetal age upon normal fetal laboratory values and venous pressure. Obstet Gynecol. 1992;79:713–8.

    CAS  PubMed  Google Scholar 

  338. Wentworth P. The placenta in cases of hemolytic disease. Am J Obstet Gynecol. 1967;98:283–9.

    CAS  PubMed  Google Scholar 

  339. Westgren M, Eastman WN, Ghandourah S, Woodhouse N. Intrauterine hypercalcaemia and non-immune hydrops fetalis – relationship to the Williams syndrome. Prenat Diagn. 1988;8:333–7.

    CAS  PubMed  Google Scholar 

  340. Whitington PF. Gestational alloimmune liver disease and neonatal hemochromatosis. Semin Liver Dis. 2012;32:325–32.

    CAS  PubMed  Google Scholar 

  341. Widness JA, Susa JB, Garcia JF, Singer DB, Sehgal P, Oh W, Schwartz R, Schwartz HC. Increased erythropoiesis and elevated erythropoietin in infants born to diabetic mothers and in hyperinsulinemic rhesus fetuses. J Clin Invest. 1981;67:637–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  342. Wiggins JW, Bowes W, Clewell W, Manco-Johnson M, Manchester D, Johnson R, Appareti K, Wolfe RR. Echocardiographic diagnosis and intravenous digoxin management of fetal tachyarrhythmias and congestive heart failure. Am J Dis Child. 1986;140:202–4.

    PubMed  Google Scholar 

  343. Windebank KP, Bridges NA, Ostman-Smith I, Stevens JE. Hydrops fetalis due to abnormal lymphatics. Arch Dis Child. 1987;62:198–200.

    CAS  PubMed  PubMed Central  Google Scholar 

  344. Wlodarski MW, Da Costa L, O'Donohue MF, Gastou M, Karboul N, Montel-Lehry N, Hainmann I, Danda D, Szvetnik A, Pastor V, Paolini N, di Summa FM, Tamary H, Quider AA, Aspesi A, Houtkooper RH, Leblanc T, Niemeyer CM, Gleizes PE, MacInnes AW. Recurring mutations in RPL15 are linked to hydrops fetalis and treatment independence in Diamond-Blackfan anemia. Haematologica. 2018;103:949–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  345. Wright JR Jr, Van den Hof MC, Macken MB. Prenatal infantile cortical hyperostosis (Caffey's disease): a 'hepatic myeloid hyperplasia-pulmonary hypoplasia sequence' can explain the lethality of early onset cases. Prenat Diagn. 2005;25(10):939–44.

    PubMed  Google Scholar 

  346. Wu Y, Chen D, Xu X, Mai M, Ye X, Li C, Santoso S, Xia W, Fu Y. Hydrops fetalis associated with anti-CD36 antibodies in fetal and neonatal alloimmune thrombocytopenia: possible underlying mechanism. Transfus Med. 2020;30:361–8.

    PubMed  Google Scholar 

  347. Yagihashi N, Watanabe K, Yagihashi S. Transient abnormal myelopoiesis accompanied by hepatic fibrosis in two infants with Down syndrome. J Clin Pathol. 1995;48:973–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  348. Younis JS, Granat M. Insufficient transplacental digoxin transfer in severe hydrops fetalis. Am J Obstet Gynecol. 1987;157:1268–9.

    CAS  PubMed  Google Scholar 

  349. Yuan SM. Cardiac etiologies of hydrops fetalis. Z Geburtshilfe Neonatol. 2017;221:67–72.

    PubMed  Google Scholar 

  350. Zanardini C, Papageorghiou A, Bhide A, Thilaganathan B. Giant placental chorioangioma: natural history and pregnancy outcome. Ultrasound Obstet Gynecol. 2010;35:332–6.

    CAS  PubMed  Google Scholar 

  351. Zhang J, Li J, Saucier JB, Feng Y, Jiang Y, Sinson J, McCombs AK, Schmitt ES, Peacock S, Chen S, Dai H, Ge X, Wang G, Shaw CA, Mei H, Breman A, Xia F, Yang Y, Purgason A, Pourpak A, Chen Z, Wang X, Wang Y, Kulkarni S, Choy KW, Wapner RJ, Van den Veyver IB, Beaudet A, Parmar S, Wong LJ, Eng CM. Non-invasive prenatal sequencing for multiple Mendelian monogenic disorders using circulating cell-free fetal DNA. Nat Med. 2019;25:439–47. Erratum in: Nat Med. 2019 Feb 20.

    CAS  PubMed  Google Scholar 

  352. Zizka Z, Fait T, Belosovicova H, Haakova L, Mara M, Jirkovska M, Jirasek JE, Bartosova L, Calda P. ABO fetomaternal compatibility poses a risk for massive fetomaternal transplacental hemorrhage. Acta Obstet Gynecol Scand. 2008;87:1011–4.

    PubMed  Google Scholar 

  353. Zonneveld R, van der Meer-Kapelle L, Sylva M, Brand A, Zijlstra M, Schonewille H. Severe fetal hemolysis and cholestasis due to high-titer maternal IgG anti-a antibodies. Pediatrics. 2019;143(4):e20182859.

    PubMed  Google Scholar 

  354. Zurbriggen K, Schmugge M, Schmid M, Durka S, Kleinert P, Kuster T, Heizmann CW, Troxler H. Analysis of minor hemoglobins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Clin Chem. 2005;51:989–96.

    CAS  PubMed  Google Scholar 

  355. Zwi LJ, Becroft DMO. Intrauterine aplastic anemia and fetal hydrops: a case report. Pediatr Pathol. 1986;5:199–205.

    CAS  PubMed  Google Scholar 

  356. Zwiers C, Lindenburg ITM, Klumper FJ, de Haas M, Oepkes D, Van Kamp IL. Complications of intrauterine intravascular blood transfusion: lessons learned after 1678 procedures. Ultrasound Obstet Gynecol. 2017;50:180–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  357. Zwiers C, van der Bom JG, van Kamp IL, van Geloven N, Lopriore E, Smoleniec J, Devlieger R, Sim PE, Ledingham MA, Tiblad E, Moise KJ Jr, Gloning KP, Kilby MD, Overton TG, Jørgensen DS, Schou KV, Paek B, Walker M, Parry E, Oepkes D, de Haas M. Postponing early intrauterine transfusion with intravenous immunoglobulin treatment; the PETIT study on severe hemolytic disease of the fetus and newborn. Am J Obstet Gynecol. 2018;219(3):291.

    Google Scholar 

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  1. Cleveland Clinic, Pathology and Laboratory Medicine Institute, Cleveland, OH, USA

    Amy Heerema-McKenney

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  1. Amy Heerema-McKenney
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Correspondence to Amy Heerema-McKenney .

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  1. Professor of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York Presbyterian Hospital, New York, NY, USA

    Rebecca N. Baergen

  2. Centre for Trophoblast Research, University of Cambridge, Cambridge, UK

    Graham J. Burton

  3. Professor Emeritus of Pathology, State University of New York, Stony Brook, NY, USA

    Cynthia G. Kaplan

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Heerema-McKenney, A. (2022). Erythroblastosis Fetalis, Hydrops Fetalis, and Transplacental Hemorrhage. In: Baergen, R.N., Burton, G.J., Kaplan, C.G. (eds) Benirschke's Pathology of the Human Placenta. Springer, Cham. https://doi.org/10.1007/978-3-030-84725-8_23

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