Heterotaxy Syndrome with Increased Nuchal Translucency and Normal Karyotype Associated with Complex Systemic Venous Return. Ultrasound Diagnosis with Autopsy Correlation

References

• Nicolaides KH, Azar G, Byrne D, Mansur C, Marks K. Fetal nuchal translucency: ultrasound screening for chromosomal defects in first trimester of pregnancy. BMJ. 1992;304(6831):867–9. doi:10.1136/bmj.304.6831.867.
   PubMed Web of Science ®Google Scholar
• Lee KA, Williams B, Roza K, Ferguson H, David K, Eddleman K, Stone J, Edelmann L, Richard G, Gelb BD, et al. PTPN11 analysis for the prenatal diagnosis of Noonan syndrome in fetuses with abnormal ultrasound findings. Clin Genet. 2009;75(2):190–4. doi:10.1111/j.1399-0004.2008.01085.x.
   PubMed Web of Science ®Google Scholar
• Souka AP, Snijders RJ, Novakov A, Soares W, Nicolaides KH. Defects and syndromes in chromosomally normal fetuses with increased nuchal translucency thickness at 10–14 weeks of gestation. Ultrasound Obstet Gynecol. 1998;11(6):391–400. doi:10.1046/j.1469-0705.1998.11060391.x.
   PubMed Web of Science ®Google Scholar
• Hyett J, Perdu M, Sharland G, Snijders R, Nicolaides KH. Using fetal nuchal translucency to screen for major congenital cardiac defects at 10-14 weeks of gestation: population based cohort study. BMJ. 1999;318(7176):81–5. doi:10.1136/bmj.318.7176.81.
   PubMed Web of Science ®Google Scholar
• Ghi T, Huggon IC, Zosmer N, Nicolaides KH. Incidence of major structural cardiac defects associated with increased nuchal translucency but normal karyotype. Ultrasound Obstet Gynecol. 2001;18(6):610–4. doi:10.1046/j.0960-7692.2001.00584.x.
   PubMed Web of Science ®Google Scholar
• Clur SA, Mathijssen IB, Pajkrt E, Cook A, Laurini RN, Ottenkamp J, Bilardo CM. Structural heart defects associated with an increased nuchal translucency: 9 years experience in a referral centre. Prenat Diagn. 2008;28(4):347–54. doi:10.1002/pd.1985.
   PubMed Web of Science ®Google Scholar
• Lopes LM, Brizot ML, Lopes MAB, Ayello VD, Schultz R, Zugaib M. Structural and functional cardiac abnormalities identified prior to 16 weeks’ gestation in fetuses with increased nuchal translucency. Ultrasound Obstet Gynecol. 2003;22(5):470–8. doi:10.1002/uog.905.
   PubMed Web of Science ®Google Scholar
• Sotiriadis A, Papatheodorou S, Eleftheriades M, Makrydimas G. Nuchal translucency and major congenital heart defects in fetuses with normal karyotype: a meta-analysis. Ultrasound Obstet Gynecol. 2013;42(4):383–9. doi:10.1002/uog.12488.
   PubMed Web of Science ®Google Scholar
• Makrydimas G, Sotiriadis A, Ioannidis JP. Screening performance of first-trimester nuchal translucency for major cardiac defects: a meta-analysis. Am J Obstet Gynecol. 2003;189(5):1330–5. doi:10.1067/s0002-9378(03)00645-8.
   PubMed Web of Science ®Google Scholar
• Michailidis GD, Economides DL. Nuchal translucency measurement and pregnancy outcome in karyotypically normal fetuses. Ultrasound Obstet Gynecol. 2001;17(2):102–5. doi:10.1046/j.1469-0705.2001.00341.x.
   PubMed Web of Science ®Google Scholar
• Westin M, Saltvedt S, Almström H, Grunewald C, Valentin L. By how much does increased nuchal translucency increase the risk of adverse pregnancy outcome in chromosomally normal fetuses? A study of 16,260 fetuses derived from an unselected pregnant population. Ultrasound Obstet Gynecol. 2007;29(2):150–8. doi:10.1002/uog.3905.
   PubMed Web of Science ®Google Scholar
• Paladini D, Pistorio A, Wu LH, Meccariello G, Lei T, Tuo G, Donarini G, Marasini M, Xie H-N. Prenatal diagnosis of total and partial anomalous pulmonary venous connection: multicenter cohort study and meta-analysis. Ultrasound Obstet Gynecol. 2018;52(1):24–34. doi:10.1002/uog.18907.
   PubMed Web of Science ®Google Scholar
• Kagan KO, Avgidou K, Molina FS, Gajewska K, Nicolaides KH. Relation between increased fetal nuchal translucency thickness and chromosomal defects. Obstet Gynecol. 2006;107(1):6–10. doi:10.1097/01.AOG.0000191301.63871.c6.
   PubMed Web of Science ®Google Scholar
• Hillman SC, Pretlove S, Coomarasamy A, McMullan DJ, Davison EV, Maher ER, Kilby MD. Additional information from array comparative genomic hybridization technology over conventional karyotyping in prenatal diagnosis: a systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2011;37(1):6–14. doi:10.1002/uog.7754.
   PubMed Web of Science ®Google Scholar
• Bilardo CM, Müller MA, Pajkrt E, Clur SA, van Zalen MM, Bijlsma EK. Increased nuchal translucency thickness and normal karyotype: time for parental reassurance. Ultrasound Obstet Gynecol. 2007;30(1):11–8. doi:10.1002/uog.4044.
   PubMed Web of Science ®Google Scholar
• Maymon R, Herman A. The clinical evaluation and pregnancy outcome of euploid fetuses with increased nuchal translucency. Clin Genet. 2004;66(5):426–36. doi:10.1111/j.1399-0004.2004.00332.x.
   PubMed Web of Science ®Google Scholar
• Souka AP, Von Kaisenberg CS, Hyett JA, Sonek JD, Nicolaides KH. Increased nuchal translucency with normal karyotype. Am J Obstet Gynecol. 2005;192(4):1005–21. doi:10.1016/j.ajog.2004.12.093.
   PubMed Web of Science ®Google Scholar
• Hyett J, Moscoso G, Papapanagiotou G, Perdu M, Nicolaides KH. Abnormalities of the heart and great arteries in chromosomally normal fetuses with increased nuchal translucency thickness at 11-13 weeks of gestation. Ultrasound Obstet Gynecol. 1996;7(4):245–50. doi:10.1046/j.1469-0705.1996.07040245.x.
   PubMed Web of Science ®Google Scholar
• Minnella GP, Crupano FM, Syngelaki A, Zidere V, Akolekar R, Nicolaides KH. Diagnosis of major heart defects by routine first-trimester ultrasound examination: association with increased nuchal translucency, tricuspid regurgitation and abnormal flow in ductus venosus. Ultrasound Obstet Gynecol. 2020;55(5):637–44. doi:10.1002/uog.21956.
   PubMed Web of Science ®Google Scholar
• Taketazu M, Lougheed J, Yoo S-J, Lim JSL, Hornberger LK. Spectrum of cardiovascular disease, accuracy of diagnosis, and outcome in fetal heterotaxy syndrome. Am J Cardiol. 2006;97(5):720–4. doi:10.1016/j.amjcard.2005.09.119.
   PubMed Web of Science ®Google Scholar
• Escobar-Diaz MC, Tworetzky W, Friedman K, Lafranchi T, Fynn-Thompson F, Alexander ME, Mah DY. Perinatal outcome in fetuses with heterotaxy syndrome and atrioventricular block or bradycardia. Pediatr Cardiol. 2014;35(6):906–13. doi:10.1007/s00246-014-0874-x.
   PubMed Web of Science ®Google Scholar
• Gottschalk I, Berg C, Heller R. Disorders of laterality and heterotaxy in the foetus. Z Geburtshilfe Neonatal. 2012;216:122–31.
   PubMed Web of Science ®Google Scholar
• Cohen MS, Schultz AH, Tian Z-Y, Donaghue DD, Weinberg PM, Gaynor JW, Rychik J. Heterotaxy syndrome with functional single ventricle: does prenatal diagnosis improve survival? Ann Thorac Surg. 2006;82(5):1629–36. doi:10.1016/j.athoracsur.2006.05.039.
   PubMed Web of Science ®Google Scholar
• Jaeggi ET, Hornberger LK, Smallhorn JF, Fouron J-C. Prenatal diagnosis of complete atrioventricular block associated with structural heart disease: combined experience of two tertiary care centers and review of the literature. Ultrasound Obstet Gynecol. 2005;26(1):16–7. doi:10.1002/uog.1919.
   PubMed Web of Science ®Google Scholar
• Schmidt KG, Ulmer HE, Silverman NH, Kleinman CS, Copel JA. Perinatal outcome of fetal complete atrioventricular block: a multicenter experience. J Am Coll Cardio.l. 1991;17(6):1360–6. doi:10.1016/S0735-1097(10)80148-2.
   PubMed Web of Science ®Google Scholar
• Berg C, Geipel A, Kamil D, Knüppel M, Breuer J, Krapp M, Baschat A, Germer U, Hansmann M, Gembruch U, et al. The syndrome of left isomerism: sonographic findings and outcome in prenatally diagnosed cases. J Ultrasound Med. 2005;24(7):921–31. doi:10.7863/jum.2005.24.7.921.
   PubMed Web of Science ®Google Scholar
• Galindo A, Gutiérrez-Larraya F, Escribano D, Arbues J, Velasco JM. Clinical significance of persistent left superior vena cava diagnosed in fetal life. Ultrasound Obstet Gynecol. 2007;30(2):152–61. doi:10.1002/uog.4045.
   PubMed Web of Science ®Google Scholar
• Berg C, Geipel A, Smrcek J, Krapp M, Germer U, Kohl T, Gembruch U, Baschat AA. Prenatal diagnosis of cardiosplenic syndromes: a 10-year experience. Ultrasound Obstet Gynecol. 2003;22(5):451–9. doi:10.1002/uog.904.
   PubMed Web of Science ®Google Scholar
• Huggon IC, Cook AC, Smeeton NC, Magee AG, Sharland GK. Atrioventricular septal defects diagnosed in fetal life: associated cardiac and extra-cardiac abnormalities and outcome. J Am Coll Cardio.l. 2000;36(2):593–601. doi:10.1016/S0735-1097(00)00757-9.
   PubMed Web of Science ®Google Scholar
• Brown DL, Emerson DS, Shulman LP, Doubilet PM, Felker RE, Van Praagh S. Predicting aneuploidy in fetuses with cardiac anomalies: significance of visceral situs and noncardiac anomalies. J Ultrasound Med. 1993;12(3):153–61. doi:10.7863/jum.1993.12.3.153.
   PubMed Web of Science ®Google Scholar
• Machevin-Surugue E, David N, Verspyck E, Labadie G, Blaysat G, Durand I, Ickowicz V, Marpeau L. Dilated coronary sinus in prenatal echocardiography; identification, associations and outcome. Prenat Diagn. 2002;22(10):898–902. doi:10.1002/pd.397.
   PubMed Web of Science ®Google Scholar
• Kalache KD, Romero R, Conoscenti G, Qureshi F, Jacques SM, Chaiworapongsa T, Treadwell M, Johnson A. Prenatal diagnosis of dilated coronary sinus with persistent left superior vena cava in a fetus with trisomy 18. Prenat Diagn. 2003;23(2):108–10. doi:10.1002/pd.460.
   PubMed Web of Science ®Google Scholar
• Keleş A, Yılmaz O, Dağdeviren G, Çelik ÖY, Yücel A, Şahin D. Persistent left superior vena cava: why is prenatal diagnosis important? Fetal Ped Pathol. 2021;1–11. Online ahead of print. doi:10.1080/15513815.2021.1933662.
   Google Scholar
• Berg C, Knüppel M, Geipel A, Kohl T, Krapp M, Knöpfle G, Germer U, Hansmann M, Gembruch U. Prenatal diagnosis of persistent left superior vena cava and its associated congenital anomalies. Ultrasound Obstet Gynecol. 2006;27(3):274–80. doi:10.1002/uog.2704.
   PubMed Web of Science ®Google Scholar
• Yilmaz O, Celik OY. Prenatal diagnosis of double-outlet right ventricle with tricuspid valve atresia, anomalous pulmonary vein connection, persistent left superior vena cava, and right atrial isomerism. J Clin Ultrasound. 2021;49(3):262–4. doi:10.1002/jcu.22908.
   PubMed Web of Science ®Google Scholar
• Sheley RC, Nyberg DA, Kapur R. Azygous continuation of the interrupted inferior vena cava: a clue to prenatal diagnosis of the cardiosplenic syndromes. J Ultrasound Med. 1995;14(5):381–7. doi:10.7863/jum.1995.14.5.381.
   PubMed Web of Science ®Google Scholar
• Mantini E, Grondin CM, Lillehei CW, Edwards JE. Congenital anomalies involving the coronary sinus. Circulation. 1966;33(2):317–27.
   Web of Science ®Google Scholar
• Rein A, Nir A, Nadjari M. The coronary sinus in the fetus. Ultrasound Obstet Gynecol. 2000;15(6):468–72. doi:10.1046/j.1469-0705.2000.00142.x.
   PubMed Web of Science ®Google Scholar
• Chaoui R, Heling KS, Kalache KD. Caliber of the coronary sinus in fetuses with cardiac defects with and without left persistent superior vena cava and in growth-restricted fetuses with heart-sparing effect. Prenat Diagn. 2003;23(7):552–7. doi:10.1002/pd.626.
   PubMed Web of Science ®Google Scholar
• Papa M, Camesasca C, Santoro F, Zoia E, Fragasso G, Giannico S, Chierchia SL. Fetal echocardiography in detecting anomalous pulmonary venous connection: four false positive cases. Br Heart J. 1995;73(4):355–8. doi:10.1136/hrt.73.4.355.
   PubMedGoogle Scholar
• Van Praagh S, Kreutzer J, Alday L, et al. Systemic and pulmonary venous connections in visceral heterotaxy, with emphasis on the diagnosis of the atrial situs: a study of 109 post-mortem cases. In: Takao A, Clark EB , editors. Developmental cardiology: morphogenesis and function. 1st ed. Mount Kisco (NY): Futura Publishing Co., Inc.; 1990. p. 671–727.
   Google Scholar
• Jacobs JP, Anderson RH, Weinberg PM, Walters HL, Tchervenkov CI, Duca DD, Franklin RCG, Aiello VD, Béland MJ, Colan SD, et al. The nomenclature, definition, and classification of cardiac structures in the setting of heterotaxy. Cardiol Young. 2007;17(S4):1–28. doi:10.1017/S1047951107001138.
   PubMedGoogle Scholar
• Niszczota C, Koleśnik A, Szymkiewicz-Dangel J. Diagnostic problems in fetal visceral heterotaxy syndrome. Sonography vs. autopsy. Cor Vasa. 2012;54(9–10):e329–e35. doi:10.1016/j.crvasa.2012.07.002.
   Google Scholar
• Routhu M, Mohammad IA. Pre natal evaluation of heterotaxy syndrome by fetal echocardiography and correlating with autopsy. Ultrasound. 2019;27(2):111–21. doi:10.1177/1742271X19836259.
   PubMed Web of Science ®Google Scholar
• Burton EC, Olson M, Rooper L. Defects in laterality with emphasis on heterotaxy syndromes with asplenia and polysplenia: an autopsy case series at a single institution. Pediatr Dev Pathol. 2014;17(4):250–64. doi:10.2350/13-11-1406-OA.1.
   PubMed Web of Science ®Google Scholar
• Struksnaes C, Blaas HK, Eik-Nes SH, Tegnander E, Vogt C. Postmortem assessment of isolated congenital heart defects remains essential following termination of pregnancy. Pediatr Dev Pathol. 2021;24(5):422–9. doi:10.1177/10935266211016184.
   PubMed Web of Science ®Google Scholar
• Salvesen KA, Oyen L, Schmidt N, Malt UF, Eik-Nes SH. Eik-Nes SH. Comparison of long-term psychological responses of women after pregnancy termination due to fetal anomalies and after perinatal loss. Ultrasound Obstet Gynecol. 1997;9(2):80–5. doi:10.1046/j.1469-0705.1997.09020080.x.
   PubMed Web of Science ®Google Scholar
• Boyd PA, Tondi F, Hicks NR, Chamberlain PF. Autopsy after termination of pregnancy for fetal anomaly: retro-spective cohort study. BMJ. 2004;328(7432):137–0. doi:10.1136/bmj.37939.570104.EE.
   PubMed Web of Science ®Google Scholar