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The multisystem nature of isomerism: left isomerism complicated by Abernethy malformation and portopulmonary hypertension

Part of: Ventricular Septal Defect (VSD) Cardiac Morphology

Published online by Cambridge University Press:  18 March 2021

Megan L. Ringle Open the ORCID record for Megan L. Ringle [Opens in a new window] ,
Rohit Loomba Open the ORCID record for Rohit Loomba [Opens in a new window] ,
John C. Dykes ,
Danyal Khan Open the ORCID record for Danyal Khan [Opens in a new window] ,
David Schidlow  and
Gil Wernovsky
Megan L. Ringle*
Affiliation:
Division of Neonatal and Developmental Medicine, Lucile Packard Children’s Hospital, Stanford University School of Medicine, Palo Alto, CA, USA
Rohit Loomba
Affiliation:
Division of Cardiology, Advocate Children’s Hospital, Chicago, IL, USA Division of Cardiology, Chicago Medical School, Chicago, IL, USA
John C. Dykes
Affiliation:
Division of Cardiology, Lucile Packard Children’s Hospital, Stanford Uiversity School of Medicine, Palo Alto, CA, USA
Danyal Khan
Affiliation:
Department of Pediatric Cardiology, Nicklaus Children’s Hospital, Miami, FL, USA
David Schidlow
Affiliation:
Department of Cardiology, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA
Gil Wernovsky
Affiliation:
Divisions of Cardiac Critical Care and Pediatric Cardiology, Children’s National Hospital, Washington, DC, USA
*
Author for correspondence: M. L. Ringle, MD, MPH, Division of Neonatal and Developmental Medicine, Lucile Packard Children’s Hospital, Stanford University School of Medicine, 750 Welch Rd, Suite 315, Palo Alto, CA 94304, USA. Tel: 650-724-9954; Fax: 650-725-6581. E-mail: meganringle@gmail.com
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Abstract

Isomerism, also referred to as “heterotaxy” is a complex set of anatomic and functional perturbations. One of the most obvious manifestations of isomerism is the disturbance of organ arrangement, such that the thoracic organs are no longer asymmetric on the left and right. We report the case of a 14-year-old female in whom exercise-induced dyspnea led to a late diagnosis of left isomerism complicated by Abernethy malformation and portopulmonary hypertension. A comprehensive evaluation revealed two anatomic left lungs and hyparterial bronchi, bilateral left atria, an interrupted inferior caval vein with azygos continuation, multiple spleens, sinus node dysfunction, hepatic hypertrophy with focal nodular hyperplasia, and absence of the portal vein. Pulmonary vasodilator therapy was initiated resulting in clinical improvement. This case exhibits unique features including a late diagnosis of isomerism with Abernethy malformation and portopulmonary hypertension. The patient’s presentation, medical workup, and future treatment emphasise the importance of multidisciplinary care in children with complex multisystem disease. We review the multiple cardiac and extracardiac manifestations of isomerism.

Keywords

Isomerismheterotaxyatrial isomerismAbernethy syndrome
Type
Review
Information
Cardiology in the Young , Volume 31 , Issue 4 , April 2021 , pp. 532 - 540
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Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Loomba, RS, Hlavacek, AM, Spicer, DE, Anderson, RH. Isomerism or heterotaxy: which term leads to better understanding? Cardiol Young 2015; 25: 1037–1043.CrossRefGoogle ScholarPubMed
Jacobs, JP, Anderson, RH, Weinberg, PM, et al. The nomenclature, definition and classification of cardiac structures in the setting of heterotaxy. Cardiol Young 2007; 17(S4): 1–28.Google ScholarPubMed
Catana, A, Apostu, AP. The determination factors of left-right asymmetry disorders- a short review. Clujul Med 2017; 90: 139–146.Google ScholarPubMed
Aylsworth, AS. Clinical aspects of defects in the determination of laterality. Am J Med Genet 2001; 101: 345–355.CrossRefGoogle ScholarPubMed
Sempou, E, Khokha, MK. Genes and mechanisms of heterotaxy: patients drive the search. Curr Opin Genet Dev 2019; 56: 34–40.CrossRefGoogle ScholarPubMed
Loomba, RS, Frommelt, PC, Anderson, RH. Genetic disturbances in patients with bodily isomerism from a single center: clinical implications of affected genes and potential impact of ciliary dyskinesia. Cardiogenetics 2016; 6: 15–21.CrossRefGoogle Scholar
Loomba, RS, Ahmed, MM, Spicer, DE, Backer, CL, Anderson, RH. Manifestations of bodily isomerism. Cardiovasc Pathol 2016; 25: 173–180.CrossRefGoogle ScholarPubMed
Loomba, R, Shah, PH, Anderson, RH, Arora, Y. Radiologic considerations in heterotaxy: the need for detailed anatomic evaluation. Curēus Palo Alto CA. 2016; 8: e470.Google ScholarPubMed
Newman, B, Feinstein, JA, Cohen, RA, et al. Congenital extrahepatic portosystemic shunt associated with heterotaxy and polysplenia. Pediatr Radiol 2010; 40: 1222–1230.CrossRefGoogle ScholarPubMed
Loomba, RS. Arterial desaturation due to pulmonary arteriovenous malformations after the Kawashima Operation. Ann Pediatr Cardiol 2016; 9: 35–38.CrossRefGoogle ScholarPubMed
Krowka, MJ, Fallon, MB, Kawut, SM, et al. International liver transplant society practice guidelines: diagnosis and management of hepatopulmonary syndrome and portopulmonary hypertension. Transplantation [Internet] 2016 Jul [cited 2020 Oct 15]; 100: 1440–1452. Retrieved from http://journals.lww.com/00007890-201607000-00013 CrossRefGoogle ScholarPubMed
Simonneau, G, Gatzoulis, MA, Adatia, I, et al. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol [Internet] 2013 Dec [cited 2020 Oct 15]; 62: D34–D41. Retrieved from https://linkinghub.elsevier.com/retrieve/pii/S0735109713058725 CrossRefGoogle ScholarPubMed
Lisovsky, M, Konstas, AA, Misdraji, J. Congenital extrahepatic portosystemic shunts (Abernethy malformation): a histopathologic evaluation. Am J Surg Pathol 2011; 35: 1381–1390.CrossRefGoogle ScholarPubMed
Savale, L, Guimas, M, Ebstein, N, et al. Portopulmonary hypertension in the current era of pulmonary hypertension management. J Hepatol [Internet] 2020 Jul [cited 2020 Oct 14]; 73: 130–139. Retrieved from https://linkinghub.elsevier.com/retrieve/pii/S0168827820301197 CrossRefGoogle ScholarPubMed
Savale, L, Watherald, J, Sitbon, O. Portopulmonary hypertension. Semin Respir Crit Care Med 2017; 38: 651–661.Google ScholarPubMed
Sitbon, O, Bosch, J, Cottreel, E, et al. Macitentan for the treatment of portopulmonary hypertension (PORTICO): a multicentre, randomised, double-blind, placebo-controlled, phase 4 trial. Lancet Respir Med [Internet] 2019 Jul [cited 2020 Oct 14]; 7: 594–604. Retrieved from https://linkinghub.elsevier.com/retrieve/pii/S2213260019300918 CrossRefGoogle ScholarPubMed
Law, YM, Mack, CL, Sokol, RJ, Rice, M, Parsley, L, Ivy, D. Cardiopulmonary manifestations of portovenous shunts from congenital absence of the portal vein: pulmonary hypertension and pulmonary vascular dilatation. Pediatr Transplant 2011; 15: E162–E168.CrossRefGoogle ScholarPubMed
Whitworth, JR, Ivy, DD, Gralla, J, Narkewicz, MR, Sokol, RJ. Pulmonary vascular complications in asymptomatic children with portal hypertension. J Pediatr Gastroenterol Nutr 2009; 49: 607–612.CrossRefGoogle ScholarPubMed
Condino, AA, Ivy, DD, O’Connor, JA, et al. Portopulmonary Hypertension in Pediatric Patients. J Pediatr 2005; 147: 20–26.CrossRefGoogle ScholarPubMed
Galiè, N, Jansa, P, Pulido, T, et al. SERAPHIN haemodynamic substudy: the effect of the dual endothelin receptor antagonist macitentan on haemodynamic parameters and NT-proBNP levels and their association with disease progression in patients with pulmonary arterial hypertension. Eur Heart J [Internet] 2017 Apr 14 [cited 2020 Oct 14]; 38: 1147–1155. Retrieved from https://academic.oup.com/eurheartj/article/38/15/1147/3058510 CrossRefGoogle ScholarPubMed
Loomba, RS. Prevalence of isomerism from a European registry: live births, fetal deaths, and terminations of pregnancy. Congenit Anom 2016; 56: 256–277.CrossRefGoogle ScholarPubMed
Evans, WN, Acherman, RJ, Restrepo, H. Heterotaxy in Southern Nevada: prenatal detection and epidemiology. Pediatr Cardiol 2015; 36: 930–934.CrossRefGoogle ScholarPubMed
Lin, AE, Krikov, S, Riehle-Colarusso, T, et al. Laterality defects in the national birth defects prevention study (1998–2007): Birth prevalence and descriptive epidemiology. Am J Med Genet A 2014; 164: 2581–2591.CrossRefGoogle Scholar
Gabriel, GC, Lo, CW. Left–right patterning in congenital heart disease beyond heterotaxy. Am J Med Genet C Semin Med Genet 2020; 184: 90–96.CrossRefGoogle ScholarPubMed
Loomba, RS, Frommelt, PC. Predictors of mortality in patients with isomerism. J Pediatr Care [Internet] 2016 [cited 2020 Oct 12]; 2. Retrieved from http://pediatrics.imedpub.com/predictors-of-mortality-in-patients-with-isomerism.php?aid=11367 CrossRefGoogle Scholar
Loomba, RS, Nijhawan, K, Anderson, R. Impact of era, type of isomerism, and ventricular morphology on survival in heterotaxy: implications for therapeutic management. World J Pediatr Congenit Heart Surg 2016; 7: 54–62.CrossRefGoogle ScholarPubMed
Brown, KL, Ridout, DA, Goldman, AP, Hoskote, A, Penny, DJ. Risk factors for long intensive care unit stay after cardiopulmonary bypass in children. Crit Care Med 2003; 31: 28–33.CrossRefGoogle ScholarPubMed
Chen, W, Ma, L, Cui, H, et al. Early-and middle-term surgical outcomes in patients with heterotaxy syndrome. Cardiology 2016; 133: 141–146.CrossRefGoogle ScholarPubMed
Gentles, TL, Mayer, JE Jr, Gauvreau, K, et al. Fontan operation in five hundred consecutive patients: factors influencing early and late outcome. J Thorac Cardiovasc Surg 1997; 114: 376–391.CrossRefGoogle ScholarPubMed
Lee, TM, Aiyagari, R, Hirsch, JC, Ohye, RG, Bove, EL, Devaney, EJ. Risk factor analysis for second-stage palliation of single ventricle anatomy. Ann Thorac Surg 2012; 93: 614–619.CrossRefGoogle ScholarPubMed
Sinzobahamvya, N, Arenz, C, Reckers, J, et al. Poor outcome for patients with totally anomalous pulmonary venous connection and functionally single ventricle. Cardiol Young 2009; 19: 594–600.CrossRefGoogle ScholarPubMed
Song, J, Kang, I-S, Huh, J, et al. Interstage mortality for functional single ventricle with heterotaxy syndrome: a retrospective study of the clinical experience of a single tertiary center. J Cardiothorac Surg 2013; 8: 93–93.CrossRefGoogle ScholarPubMed
Stamm, C, Friehs, I, Mayer, JE Jr, et al. Long-term results of the lateral tunnel Fontan operation. J Thorac Cardiovasc Surg 2001; 121: 28–41.CrossRefGoogle ScholarPubMed
Wolff, D, van Melle, JP, Ebels, T, Hillege, H, van Slooten, YJ, Berger, RM. Trends in mortality (1975–2011) after one-and two-stage Fontan surgery, including bidirectional Glenn through Fontan completion. Eur J Cardiothorac Surg 2014; 45: 602–609.CrossRefGoogle ScholarPubMed
Zou, M, Wang, Y, Cui, H, et al. Outcomes of total cavopulmonary connection for single ventricle palliation. J Thorac Dis 2016; 8: 43.Google ScholarPubMed
Uemura, H, Ho, SY, Devine, WA, Anderson, RH. Analysis of visceral heterotaxy according to splenic status, appendage morphology, or both. Am J Cardiol 1995; 76: 846–849.CrossRefGoogle ScholarPubMed
Uemura, H, Ho, SY, Devine, WA, Kilpatrick, LL, Anderson, RH. Atrial appendages and venoatrial connections in hearts from patients with visceral heterotaxy. Ann Thorac Surg 1995; 60: 561–569.CrossRefGoogle ScholarPubMed
Anderson, RH, Spicer, DE, Loomba, R. Is an appreciation of isomerism the key to unlocking the mysteries of the cardiac findings in heterotaxy? J Cardiovasc Dev Dis 2018; 5: 11.CrossRefGoogle ScholarPubMed
Mori, S, Anderson, RH, Nishii, T, Matsumoto, K, Loomba, RS. Isomerism in the setting of the so-called “heterotaxy”: the usefulness of computed tomographic analysis. Ann Pediatr Cardiol 2017; 10: 175.CrossRefGoogle ScholarPubMed
Tremblay, C, Loomba, RS, Frommelt, PC, et al. Segregating bodily isomerism or heterotaxy: potential echocardiographic correlations of morphological findings. Cardiol Young 2017; 27: 1470.CrossRefGoogle ScholarPubMed
Ozawa, Y, Asakai, H, Shiraga, K, et al. Cardiac rhythm disturbances in heterotaxy syndrome. Pediatr Cardiol 2019; 40: 909–913.CrossRefGoogle ScholarPubMed
Loomba, RS, Willes, RJ, Kovach, JR, Anderson, RH. Chronic arrhythmias in the setting of heterotaxy: differences between right and left isomerism. Congenit Heart Dis 2016; 11: 7–18.CrossRefGoogle ScholarPubMed
Loomba, RS, Aggarwal, S, Gupta, N, et al. Arrhythmias in adult congenital patients with bodily isomerism. Pediatr Cardiol 2016; 37: 330–337.CrossRefGoogle ScholarPubMed
Niu, MC, Dickerson, HA, Moore, JA, et al. Heterotaxy syndrome and associated arrhythmias in pediatric patients. Heart Rhythm 2018; 15: 548–554.CrossRefGoogle ScholarPubMed
Eronen, MP, Aittomäki, KA, Kajantie, EO, Sairanen, HI, Pesonen, EJ. The outcome of patients with right atrial isomerism is poor. Pediatr Cardiol 2013; 34: 302–307.CrossRefGoogle ScholarPubMed
Wu, M-H, Wang, J-K, Lin, J-L, et al. Supraventricular tachycardia in patients with right atrial isomerism. J Am Coll Cardiol 1998; 32: 773–779.CrossRefGoogle ScholarPubMed
Cheung, Y, Cheng, VY, Yung, T, Chau, AK. Cardiac rhythm and symptomatic arrhythmia in right atrial isomerism. Am Heart J 2002; 144: 159–164.CrossRefGoogle ScholarPubMed
Broda, CR, Salciccioli, KB, Lopez, KN, Ermis, PR, Moodie, DS, Dickerson, HA. Outcomes in adults with congenital heart disease and heterotaxy syndrome: a single-center experience. Congenit Heart Dis 2019; 14: 885–894.CrossRefGoogle ScholarPubMed
Baban, A, Cantarutti, N, Adorisio, R, et al. Long-term survival and phenotypic spectrum in heterotaxy syndrome: A 25-year follow-up experience. Int J Cardiol 2018; 268: 100–105.CrossRefGoogle ScholarPubMed
Bartram, U, Wirbelauer, J, Speer, CP. Heterotaxy syndrome–asplenia and polysplenia as indicators of visceral malposition and complex congenital heart disease. Neonatology 2005; 88: 278–290.CrossRefGoogle ScholarPubMed
Van Praagh, S, Santini, F, Sanders, SP. Cardiac malpositions with special emphasison visceral heterotaxy (asplenia and polysplenia syndromes). In: Fyler DC (ed.). Nadas’ Pediatric Cardiology. Hanley & Belfus, Philadelphia, 1992: 589–608.Google Scholar
Ticho, BS, Goldstein, AM, Van Praagh, R. Extracardiac anomalies in the heterotaxy syndromes with focus on anomalies of midline-associated structures. Am J Cardiol 2000; 85: 729–734.CrossRefGoogle ScholarPubMed
Rose, V, Izukawa, T, Moes, C. Syndromes of asplenia and polysplenia. A review of cardiac and non-cardiac malformations in 60 cases withspecial reference to diagnosis and prognosis. Heart 1975; 37: 840–852.CrossRefGoogle ScholarPubMed
Phoon, CK, Neill, CA. Asplenia syndrome: insight into embryology through an analysis of cardiac and extracardiac anomalies. Am J Cardiol 1994; 73: 581–587.CrossRefGoogle ScholarPubMed
Peoples, WM, Moller, JH, Edwards, JE. Polysplenia: a review of 146 cases. Pediatr Cardiol 1983; 4: 129–137.CrossRefGoogle ScholarPubMed
Nakhleh, N, Francis, R, Giese, RA, et al. High prevalence of respiratory ciliary dysfunction in congenital heart disease patients with heterotaxy. Circulation 2012; 125: 2232–2242.CrossRefGoogle ScholarPubMed
Kothari, SS. Non-cardiac issues in patients with heterotaxy syndrome. Ann Pediatr Cardiol 2014; 7: 187.CrossRefGoogle ScholarPubMed
Harden, B, Tian, X, Giese, R, et al. Increased postoperative respiratory complications in heterotaxy congenital heart disease patients with respiratory ciliary dysfunction. J Thorac Cardiovasc Surg 2014; 147: 1291–1298.CrossRefGoogle ScholarPubMed
Freedom, RM. The asplenia syndrome: a review of significant extracardiac structural abnormalities in 29 necropsied patients. J Pediatr 1972; 81: 1130–1133.CrossRefGoogle ScholarPubMed
Hildebrandt, F, Benzing, T, Katsanis, N. Ciliopathies. N Engl J Med 2011; 364: 1533–1543.CrossRefGoogle ScholarPubMed
Louvi, A, Grove, EA. Cilia in the CNS: the quiet organelle claims center stage. Neuron 2011; 69: 1046–1060.CrossRefGoogle ScholarPubMed
Marley, A, von Zastrow, M. A simple cell-based assay reveals that diverse neuropsychiatric risk genes converge on primary cilia. PloS One 2012; 7: e46647.CrossRefGoogle ScholarPubMed
Westland, R, Schreuder, MF, van Goudoever, JB, Sanna-Cherchi, S, van Wijk, JA. Clinical implications of the solitary functioning kidney. Clin J Am Soc Nephrol 2014; 9: 978–986.CrossRefGoogle ScholarPubMed
Gayer, G, Apter, S, Jonas, T, et al. Polysplenia syndrome detected in adulthood: report of eight cases and review of the literature. Abdom Imaging 1999; 24: 178–184.CrossRefGoogle ScholarPubMed
Applegate, KE, Goske, MJ, Pierce, G, Murphy, D. Situs revisited: imaging of the heterotaxy syndrome. Radiographics 1999; 19: 837–852.CrossRefGoogle ScholarPubMed
Chandra, RS. Biliary atresia and other structural anomalies in the congenital polysplenia syndrome. J Pediatr 1974; 85: 649–655.CrossRefGoogle ScholarPubMed
Kiuchi, M, Kawachi, Y, Kimura, Y. Sudden infant death due to asplenia syndrome. Am J Forensic Med Pathol 1988; 9: 102–104.CrossRefGoogle ScholarPubMed
Mishalany, H, Mahnovski, V, Woolley, M. Congenital asplenia and anomalies of the gastrointestinal tract. Surgery 1982; 91: 38–41.Google ScholarPubMed
Van Mierop, L, Eisen, S, Schiebler, GL. The radiographic appearance of the tracheobronchial tree as an indicator of visceral situs. Am J Cardiol 1970; 26: 432–435.CrossRefGoogle ScholarPubMed
Ryerson, LM, Pharis, S, Pockett, C, et al. Heterotaxy syndrome and intestinal rotation abnormalities. Pediatrics 2018; 142(2): e20174267.CrossRefGoogle ScholarPubMed
Torres, AM, Ziegler, MM. Malrotation of the intestine. World J Surg 1993; 17: 326–331.CrossRefGoogle ScholarPubMed
Filston, HC, Kirks, DR. Malrotation—the ubiquitous anomaly. J Pediatr Surg 1981; 16: 614–620.CrossRefGoogle Scholar
Falchetti, D, de Carvalho, FB, Clapuyt, P, et al. Liver transplantation in children with biliary atresia and polysplenia syndrome. J Pediatr Surg 1991; 26: 528–531.CrossRefGoogle ScholarPubMed
Rock, N, McLin, V. Liver involvement in children with ciliopathies. Clin Res Hepatol Gastroenterol 2014; 38: 407–414.CrossRefGoogle ScholarPubMed
Chu, AS, Russo, PA, Wells, RG. Cholangiocyte cilia are abnormal in syndromic and non-syndromic biliary atresia. Mod Pathol 2012; 25: 751–757.CrossRefGoogle ScholarPubMed
Murray, CP, Yoo, S-J, Babyn, PS. Congenital extrahepatic portosystemic shunts. Pediatr Radiol 2003; 33: 614–620.Google ScholarPubMed
McElhinney, DB, Marx, GR, Newburger, JW. Congenital portosystemic venous connections and other abdominal venous abnormalities in patients with polysplenia and functionally univentricular heart disease: a case series and literature review. Congenit Heart Dis 2011; 6: 28–40.CrossRefGoogle ScholarPubMed
Low, J, Williams, D, Chaganti, J. Polysplenia syndrome with agenesis of the dorsal pancreas and preduodenal portal vein presenting with obstructive jaundice—a case report and literature review. Br J Radiol 2011; 84(1007): e219–e222.CrossRefGoogle Scholar
Odabasi, M, Arslan, C, Abuoglu, H, et al. An unusual presentation of perforated appendicitis in epigastric region. Int J Surg Case Rep 2014; 5: 76–78.CrossRefGoogle ScholarPubMed
Ely, AB, Gorelik, N, Cohen-Sivan, Y, et al. Appendicitis in adults with incidental midgut malrotation: CT findings. Clin Radiol 2013; 68: 1212–1219.Google ScholarPubMed
Brigden, ML. Detection, education and management of the asplenic or hyposplenic patient. Am Fam Physician. 2001; 63: 499.Google ScholarPubMed
Melles, D, de Marie, S. Prevention of infections in hyposplenic and asplenic patients: an update. Neth J Med 2004; 62(2): 45–52.Google ScholarPubMed
Yamamura, K, Joo, K, Ohga, S, et al. Thrombocytosis in asplenia syndrome with congenital heart disease: a previously unrecognized risk factor for thromboembolism. Int J Cardiol 2013; 167: 2259–2263.CrossRefGoogle ScholarPubMed
Knott-Craig, CJ, Danielson, GK, Schaff, HV, Puga, FJ, Weaver, AL, Driscoll, DD. The modified Fontan operation: an analysis of risk factors for early postoperative death or takedown in 702 consecutive patients from one institution. J Thorac Cardiovasc Surg 1995; 109: 1237–1243.CrossRefGoogle ScholarPubMed
Khan, PN, Nair, RJ, Olivares, J, Tingle, LE, Li, Z. Postsplenectomy reactive thrombocytosis. In: Baylor University Medical Center Proceedings, Vol. 22, No. 1. Taylor & Francis, 2009: 9–12.Google Scholar
Diller, G-P, Kempny, A, Alonso-Gonzalez, R, et al. Survival prospects and circumstances of death in contemporary adult congenital heart disease patients under follow-up at a large tertiary centre. Circulation 2015; 132: 2118–2125.CrossRefGoogle Scholar
Bhaskar, J, Galati, JC, Brooks, P, et al. Survival into adulthood of patients with atrial isomerism undergoing cardiac surgery. J Thorac Cardiovasc Surg 2015; 149: 1509–1514.CrossRefGoogle ScholarPubMed
Escobar-Diaz, MC, Friedman, K, Salem, Y, et al. Perinatal and infant outcomes of prenatal diagnosis of heterotaxy syndrome (asplenia and polysplenia). Am J Cardiol 2014; 114: 612–617.CrossRefGoogle Scholar
Anderson, RH, Baker, EJ, Redington, A, Rigby, ML, Penny, D, Wernovsky, G. Paediatric Cardiology. Elsevier Health Sciences, 2009.Google Scholar