3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 543
CASE SERIES
Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts Susanne Jerabek-Klestil, MD, Christine Brantner, MD, Regina Nehoda, MD, Elisabeth D’Costa, MD, Silvana Campei, MD, Matthias Scheier, MD
The incidence of fetal portosystemic anastomoses is unknown, and it is presumed that many cases remain undetected, as visualization of the hepatic vasculature is not part of the routine 20-week sonographic scan in pregnancy. However, portosystemic anastomoses are associated with fetal growth restriction due to a diminished oxygen supply to hepatocytes and, hence, downregulation of liver function. In these cases, uteroplacental perfusion might be normal. Key Words—fetal growth restriction; intrauterine growth restriction; obstetric ultrasound; portocaval anastomosis; portosystemic shunt; small for gestational age
W
e report 3 cases of congenital portosystemic anastomoses and intrauterine growth restriction and recommend performing a targeted sonographic examination of the fetal hepatic vasculature in cases of unexplained fetal growth restriction.
Case Descriptions
Received April 29, 2013, from the Department of Gynecology and Obstetrics, Innsbruck Medical University, Innsbruck, Austria. Revision requested June 6, 2013. Revised manuscript accepted for publication July 11, 2013. Address correspondence to Susanne JerabekKlestil, MD, Department of Gynecology and Obstetrics, Innsbruck Medical University Hospital, Anichstrasse 35, 6020 Innsbruck, Austria. E-mail: [email protected] doi:10.7863/ultra.33.3.543
Case 1 This case was a 27-year-old woman, gravida 2, para 1. Gestational age was confirmed by first-trimester sonography. The 20-week scan revealed no obvious structural defects. Fetal growth restriction beginning at 20 gestational weeks with normal blood flow in the uterine arteries and normal arterial and venous fetal Doppler recordings was observed. The amniotic fluid volume was normal throughout the pregnancy. The fetus was regularly followed to assess the fetal growth rate, and at 34 weeks, an intrahepatic portocaval anastomosis from the left portal vein to the inferior vena cava was diagnosed. Spontaneous delivery occurred at 36 weeks 5 days, and a male neonate was born weighing 1625 g (z score, –2.91)1 with Apgar scores of 4, 6, and 7 at 1, 5, and 10 minutes, respectively, and an umbilical artery pH of 7.21. Postnatal sonography showed an intrahepatic portocaval shunt from the left branch of the portal vein to the left liver vein and signs of liver cirrhosis, which was suspected to be due to intrauterine alloimmune hepatitis. At the age of 8 months, the portosystemic shunt was spontaneously regressing, and the hepatic function remained stable.
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:543–546 | 0278-4297 | www.aium.org
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 544
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
Case 2 This case was a dichorionic twin pregnancy in a 20-yearold woman, gravida 2, para 1. Gestational age was confirmed by first-trimester screening. The 20-week scan did not reveal obvious structural defects in both normal-sized fetuses. Fetal growth restriction of fetus 1 developed from 24 gestational weeks onward, whereas the growth rate of fetus 2 remained normal. Throughout the pregnancy, the uteroplacental, umbilicoplacental, and fetal arterial blood flow and amniotic fluid volume were normal in both twins. At 33 gestational weeks, a portosystemic anastomosis arising from the left portal vein and draining into the right hepatic vein could be seen in fetus 1. The anastomosis could be visualized draining into an enlarged right hepatic vein on grayscale imaging (Figure 1A). The visualization was enhanced on color flow mapping (Figure 1B). At 34 weeks 6 days, premature preterm rupture of membranes occurred, and a cesarean delivery was performed. Two neonates were delivered: neonate 1, weighing 1170 g (z score, –3.12)1 with Apgar scores of 8, 9, and 9 and an umbilical artery pH of 7.36; and neonate 2, weighing 2715 g (z score, 0.37)1 with Apgar scores of 7, 8, and 9 and an umbilical artery pH of 7.36. Postnatal sonography showed an intrahepatic portovenous shunt in the smaller child arising from the left portal vein and draining into all 3 liver veins. Liver parenchyma and liver function were normal. Spontaneous regression of the shunt occurred after 28 days, and the infant was developing normally at the age of 5 months.
Case 3 This case was a 38-year-old woman, gravida 2, para 1. Gestational age was confirmed by first-trimester screening. Fetal growth restriction started at 21 weeks’ gestation. There was mild maternal gestational hypertension, and an increased uterine artery pulsatility index. Normal blood flow was observed in the umbilical and cerebral arteries and the ductus venosus. The amniotic fluid volume was normal throughout the pregnancy. Because of vaginal bleeding and pathologic cardiotocographic tracings, a cesarean delivery was performed at 32 weeks 3 days. A male neonate was born weighing 1150 g (z score, –2.24)1 with Apgar scores of 6, 8, and 9 and an umbilical artery pH of 7.31. Postnatal sonography revealed an intrahepatic portovenous shunt from the left portal vein to the middle liver vein. Liver parenchyma and liver function were normal. The portovenous shunt regressed, and the infant was developing normally at the age of 5 months.
Discussion The incidence of congenital portocaval anastomoses in fetuses and children is unknown. We are aware of only 1 previous case report describing a fetus with an intrahepatic portosystemic shunt, which was delivered for intrauterine growth restriction and pathologic ductus venosus blood flow in the 35th gestational week.2 A second report described a fetus with an absent portal vein and drainage of the dilated umbilical vein directly into the inferior vena cava.3 By definition, this case is not a portocaval but an umbilicocaval anastomosis.
Figure 1. Case 2 at 34 weeks 4 days. A, Grayscale depiction of a portosystemic anastomosis from the left portal vein to the right hepatic vein. B, Color flow mapping of the portosystemic anastomosis from the left portal vein to the right hepatic vein. A
544
B
J Ultrasound Med 2014; 33:543–546
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 545
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
Intrahepatic portocaval anastomoses are only detected on targeted sonography of the fetal liver, and visualization is enhanced by color flow mapping. We assume that most cases remain undetected at the 20-week anomaly scan because of the small size of the anastomoses and the fact that color Doppler investigation of the liver is not part of the routine sonographic examination. However, in cases with unexplained fetal growth restriction, a detailed examination of the fetus should include color flow mapping of the fetal liver to exclude vascular malformations. Portosystemic anastomoses present as dilated branches of the portal vein, which communicate with the liver venous system. The draining veins are increased in diameter. These shunts can be visualized best in a transverse plane of the upper abdomen, where the hepatic venous system, the ductus venosus, and the portal venous system can be examined in 3 adjacent horizontal planes.4 Although visualization might be difficult in the grayscale mode, these anastomoses are easily detected on color flow mapping. A relationship between umbilical venous blood flow, liver blood perfusion, and fetal growth has been shown previously.5–8 The human fetus adapts to uteroplacental impairment by increased shunting of well-oxygenated and nutrient-rich umbilical venous blood through the ductus venosus,9 causing reduced perfusion of the fetal liver. The decreased liver blood supply reduces cell proliferation in the fetal liver,5 and hypoxia of hepatocytes leads to reduced insulinlike growth factor production.10 It has been recently shown that in growth-restricted neonates, serum alanine aminotransferase concentrations are decreased, which is thought to indicate downregulated hepatic activity.11 Similarly to increased ductus venosus shunting in pregnancies with uteroplacental insufficiency, we hypothesize that portocaval anastomoses lead to a steal phenomenon,12 causing less perfusion of the fetal liver with oxygenenriched umbilical venous blood. Growth restriction in these cases is not caused by generalized hypo-oxygenation of fetal blood but by localized hypoperfusion of the fetal liver with oxygen-rich blood. Fetal growth restriction might not only be due to oxygen depletion of the hepatocytes but might also be due to reduced perfusion itself, with reduced supplies of nutrients and metabolic factors. For this reason, blood flow in the umbilical and cerebral arteries remains normal, as shown by normal Doppler values for these vessels in our patients. In cases in which the umbilical vein bypasses the liver and drains directly into the inferior vena cava, fetal growth seems to be normal.13 In these cases, there is no oxygen extraction by hepatocytes, and because of altered blood flow in the fetal heart, the fetal liver is supplied with blood with
J Ultrasound Med 2014; 33:543–546
a higher-than-usual oxygen content through the hepatic arteries. This condition further suggests that oxygen depletion of liver cells is a major contributor to intrauterine growth restriction in cases with portosystemic shunts. We believe that preterm delivery should not be induced in these cases because of the reduced fetal growth rate, as growth restriction is not due to uteroplacental impairment, and the fetus might therefore not benefit from early delivery. Neonates with portosystemic anastomoses might have lifethreatening metabolic disturbances14 and therefore might need surgical closure of the shunt. This factor further favors delivery at an advanced gestational age. We propose that in cases of unexplained growth restriction, a detailed examination of the fetal liver using color flow mapping should be performed to exclude portocaval anastomoses.
References 1.
Fenton TR. A new growth chart for preterm babies: Babson and Benda’s chart updated with recent data and a new format. BMC Pediatr 2003; 3:13. 2. Delle Chiaie L, Neuberger P, Von Kalle T. Congenital intrahepatic portosystemic shunt: prenatal diagnosis and possible influence on fetal growth. Ultrasound Obstet Gynecol 2008; 32:233–235. 3. Manning N, Impey L, Lindsell D, Lakhoo K. Prenatally diagnosed portocaval shunt and postnatal outcome: a case report. Prenat Diagn 2004; 24:537–540. 4. Yagel S, Kivilevitch Z, Cohen SM, et al. The fetal venous system, part I: normal embryology, anatomy, hemodynamics, ultrasound evaluation and Doppler investigation. Ultrasound Obstet Gynecol 2010; 35:741–750. 5. Tchirikov M, Kertschanska S, Sturenberg HJ, Schroder HJ. Liver blood perfusion as a possible instrument for fetal growth regulation. Placenta 2002; 23(suppl A):S153–S158. 6. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Longitudinal study of umbilical and portal venous blood flow to the fetal liver: low pregnancy weight gain is associated with preferential supply to the fetal left liver lobe. Pediatr Res 2008; 63:315–320. 7. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Fetal growth restriction is associated with prioritization of umbilical blood flow to the left hepatic lobe at the expense of the right lobe. Pediatr Res 2009; 66:113– 117. 8. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Venous liver blood flow and regulation of human fetal growth: evidence from macrosomic fetuses. Am J Obstet Gynecol 2011; 204:429.e1–429.e7. 9. Kiserud T, Kessler J, Ebbing C, Rasmussen S. Ductus venosus shunting in growth-restricted fetuses and the effect of umbilical circulatory compromise. Ultrasound Obstet Gynecol 2006; 28:143–149. 10. Popovici RM, Lu M, Bhatia S, Faessen GH, Giaccia AJ, Giudice LC. Hypoxia regulates insulin-like growth factor-binding protein 1 in human fetal hepatocytes in primary culture: suggestive molecular mechanisms for in utero fetal growth restriction caused by uteroplacental insufficiency. J Clin Endocrinol Metab 2001; 86:2653–2659. 545
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 546
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
11. Kocylowski R, Dubiel M, Gudmundsson S, Fritzer E, Kiserud T, von Kaisenberg C. Hepatic aminotransferases of normal and IUGR fetuses in cord blood at birth. Early Hum Dev 2012; 88:461–465. 12. Fisher C. A new vascular syndrome: the subclavian steal. N Engl J Med 1961; 265:912–913. 13. Hajdu J, Marton T, Kozsurek M, et al. Prenatal diagnosis of abnormal course of umbilical vein and absent ductus venosus: report of three cases. Fetal Diagn Ther 2008; 23:136–139. 14. Ferrero GB, Porta F, Biamino E, et al. Remittent hyperammonemia in congenital portosystemic shunt. Eur J Pediatr 2010; 169:369–372.
546
J Ultrasound Med 2014; 33:543–546
CASE SERIES
Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts Susanne Jerabek-Klestil, MD, Christine Brantner, MD, Regina Nehoda, MD, Elisabeth D’Costa, MD, Silvana Campei, MD, Matthias Scheier, MD
The incidence of fetal portosystemic anastomoses is unknown, and it is presumed that many cases remain undetected, as visualization of the hepatic vasculature is not part of the routine 20-week sonographic scan in pregnancy. However, portosystemic anastomoses are associated with fetal growth restriction due to a diminished oxygen supply to hepatocytes and, hence, downregulation of liver function. In these cases, uteroplacental perfusion might be normal. Key Words—fetal growth restriction; intrauterine growth restriction; obstetric ultrasound; portocaval anastomosis; portosystemic shunt; small for gestational age
W
e report 3 cases of congenital portosystemic anastomoses and intrauterine growth restriction and recommend performing a targeted sonographic examination of the fetal hepatic vasculature in cases of unexplained fetal growth restriction.
Case Descriptions
Received April 29, 2013, from the Department of Gynecology and Obstetrics, Innsbruck Medical University, Innsbruck, Austria. Revision requested June 6, 2013. Revised manuscript accepted for publication July 11, 2013. Address correspondence to Susanne JerabekKlestil, MD, Department of Gynecology and Obstetrics, Innsbruck Medical University Hospital, Anichstrasse 35, 6020 Innsbruck, Austria. E-mail: [email protected] doi:10.7863/ultra.33.3.543
Case 1 This case was a 27-year-old woman, gravida 2, para 1. Gestational age was confirmed by first-trimester sonography. The 20-week scan revealed no obvious structural defects. Fetal growth restriction beginning at 20 gestational weeks with normal blood flow in the uterine arteries and normal arterial and venous fetal Doppler recordings was observed. The amniotic fluid volume was normal throughout the pregnancy. The fetus was regularly followed to assess the fetal growth rate, and at 34 weeks, an intrahepatic portocaval anastomosis from the left portal vein to the inferior vena cava was diagnosed. Spontaneous delivery occurred at 36 weeks 5 days, and a male neonate was born weighing 1625 g (z score, –2.91)1 with Apgar scores of 4, 6, and 7 at 1, 5, and 10 minutes, respectively, and an umbilical artery pH of 7.21. Postnatal sonography showed an intrahepatic portocaval shunt from the left branch of the portal vein to the left liver vein and signs of liver cirrhosis, which was suspected to be due to intrauterine alloimmune hepatitis. At the age of 8 months, the portosystemic shunt was spontaneously regressing, and the hepatic function remained stable.
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:543–546 | 0278-4297 | www.aium.org
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 544
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
Case 2 This case was a dichorionic twin pregnancy in a 20-yearold woman, gravida 2, para 1. Gestational age was confirmed by first-trimester screening. The 20-week scan did not reveal obvious structural defects in both normal-sized fetuses. Fetal growth restriction of fetus 1 developed from 24 gestational weeks onward, whereas the growth rate of fetus 2 remained normal. Throughout the pregnancy, the uteroplacental, umbilicoplacental, and fetal arterial blood flow and amniotic fluid volume were normal in both twins. At 33 gestational weeks, a portosystemic anastomosis arising from the left portal vein and draining into the right hepatic vein could be seen in fetus 1. The anastomosis could be visualized draining into an enlarged right hepatic vein on grayscale imaging (Figure 1A). The visualization was enhanced on color flow mapping (Figure 1B). At 34 weeks 6 days, premature preterm rupture of membranes occurred, and a cesarean delivery was performed. Two neonates were delivered: neonate 1, weighing 1170 g (z score, –3.12)1 with Apgar scores of 8, 9, and 9 and an umbilical artery pH of 7.36; and neonate 2, weighing 2715 g (z score, 0.37)1 with Apgar scores of 7, 8, and 9 and an umbilical artery pH of 7.36. Postnatal sonography showed an intrahepatic portovenous shunt in the smaller child arising from the left portal vein and draining into all 3 liver veins. Liver parenchyma and liver function were normal. Spontaneous regression of the shunt occurred after 28 days, and the infant was developing normally at the age of 5 months.
Case 3 This case was a 38-year-old woman, gravida 2, para 1. Gestational age was confirmed by first-trimester screening. Fetal growth restriction started at 21 weeks’ gestation. There was mild maternal gestational hypertension, and an increased uterine artery pulsatility index. Normal blood flow was observed in the umbilical and cerebral arteries and the ductus venosus. The amniotic fluid volume was normal throughout the pregnancy. Because of vaginal bleeding and pathologic cardiotocographic tracings, a cesarean delivery was performed at 32 weeks 3 days. A male neonate was born weighing 1150 g (z score, –2.24)1 with Apgar scores of 6, 8, and 9 and an umbilical artery pH of 7.31. Postnatal sonography revealed an intrahepatic portovenous shunt from the left portal vein to the middle liver vein. Liver parenchyma and liver function were normal. The portovenous shunt regressed, and the infant was developing normally at the age of 5 months.
Discussion The incidence of congenital portocaval anastomoses in fetuses and children is unknown. We are aware of only 1 previous case report describing a fetus with an intrahepatic portosystemic shunt, which was delivered for intrauterine growth restriction and pathologic ductus venosus blood flow in the 35th gestational week.2 A second report described a fetus with an absent portal vein and drainage of the dilated umbilical vein directly into the inferior vena cava.3 By definition, this case is not a portocaval but an umbilicocaval anastomosis.
Figure 1. Case 2 at 34 weeks 4 days. A, Grayscale depiction of a portosystemic anastomosis from the left portal vein to the right hepatic vein. B, Color flow mapping of the portosystemic anastomosis from the left portal vein to the right hepatic vein. A
544
B
J Ultrasound Med 2014; 33:543–546
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 545
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
Intrahepatic portocaval anastomoses are only detected on targeted sonography of the fetal liver, and visualization is enhanced by color flow mapping. We assume that most cases remain undetected at the 20-week anomaly scan because of the small size of the anastomoses and the fact that color Doppler investigation of the liver is not part of the routine sonographic examination. However, in cases with unexplained fetal growth restriction, a detailed examination of the fetus should include color flow mapping of the fetal liver to exclude vascular malformations. Portosystemic anastomoses present as dilated branches of the portal vein, which communicate with the liver venous system. The draining veins are increased in diameter. These shunts can be visualized best in a transverse plane of the upper abdomen, where the hepatic venous system, the ductus venosus, and the portal venous system can be examined in 3 adjacent horizontal planes.4 Although visualization might be difficult in the grayscale mode, these anastomoses are easily detected on color flow mapping. A relationship between umbilical venous blood flow, liver blood perfusion, and fetal growth has been shown previously.5–8 The human fetus adapts to uteroplacental impairment by increased shunting of well-oxygenated and nutrient-rich umbilical venous blood through the ductus venosus,9 causing reduced perfusion of the fetal liver. The decreased liver blood supply reduces cell proliferation in the fetal liver,5 and hypoxia of hepatocytes leads to reduced insulinlike growth factor production.10 It has been recently shown that in growth-restricted neonates, serum alanine aminotransferase concentrations are decreased, which is thought to indicate downregulated hepatic activity.11 Similarly to increased ductus venosus shunting in pregnancies with uteroplacental insufficiency, we hypothesize that portocaval anastomoses lead to a steal phenomenon,12 causing less perfusion of the fetal liver with oxygenenriched umbilical venous blood. Growth restriction in these cases is not caused by generalized hypo-oxygenation of fetal blood but by localized hypoperfusion of the fetal liver with oxygen-rich blood. Fetal growth restriction might not only be due to oxygen depletion of the hepatocytes but might also be due to reduced perfusion itself, with reduced supplies of nutrients and metabolic factors. For this reason, blood flow in the umbilical and cerebral arteries remains normal, as shown by normal Doppler values for these vessels in our patients. In cases in which the umbilical vein bypasses the liver and drains directly into the inferior vena cava, fetal growth seems to be normal.13 In these cases, there is no oxygen extraction by hepatocytes, and because of altered blood flow in the fetal heart, the fetal liver is supplied with blood with
J Ultrasound Med 2014; 33:543–546
a higher-than-usual oxygen content through the hepatic arteries. This condition further suggests that oxygen depletion of liver cells is a major contributor to intrauterine growth restriction in cases with portosystemic shunts. We believe that preterm delivery should not be induced in these cases because of the reduced fetal growth rate, as growth restriction is not due to uteroplacental impairment, and the fetus might therefore not benefit from early delivery. Neonates with portosystemic anastomoses might have lifethreatening metabolic disturbances14 and therefore might need surgical closure of the shunt. This factor further favors delivery at an advanced gestational age. We propose that in cases of unexplained growth restriction, a detailed examination of the fetal liver using color flow mapping should be performed to exclude portocaval anastomoses.
References 1.
Fenton TR. A new growth chart for preterm babies: Babson and Benda’s chart updated with recent data and a new format. BMC Pediatr 2003; 3:13. 2. Delle Chiaie L, Neuberger P, Von Kalle T. Congenital intrahepatic portosystemic shunt: prenatal diagnosis and possible influence on fetal growth. Ultrasound Obstet Gynecol 2008; 32:233–235. 3. Manning N, Impey L, Lindsell D, Lakhoo K. Prenatally diagnosed portocaval shunt and postnatal outcome: a case report. Prenat Diagn 2004; 24:537–540. 4. Yagel S, Kivilevitch Z, Cohen SM, et al. The fetal venous system, part I: normal embryology, anatomy, hemodynamics, ultrasound evaluation and Doppler investigation. Ultrasound Obstet Gynecol 2010; 35:741–750. 5. Tchirikov M, Kertschanska S, Sturenberg HJ, Schroder HJ. Liver blood perfusion as a possible instrument for fetal growth regulation. Placenta 2002; 23(suppl A):S153–S158. 6. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Longitudinal study of umbilical and portal venous blood flow to the fetal liver: low pregnancy weight gain is associated with preferential supply to the fetal left liver lobe. Pediatr Res 2008; 63:315–320. 7. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Fetal growth restriction is associated with prioritization of umbilical blood flow to the left hepatic lobe at the expense of the right lobe. Pediatr Res 2009; 66:113– 117. 8. Kessler J, Rasmussen S, Godfrey K, Hanson M, Kiserud T. Venous liver blood flow and regulation of human fetal growth: evidence from macrosomic fetuses. Am J Obstet Gynecol 2011; 204:429.e1–429.e7. 9. Kiserud T, Kessler J, Ebbing C, Rasmussen S. Ductus venosus shunting in growth-restricted fetuses and the effect of umbilical circulatory compromise. Ultrasound Obstet Gynecol 2006; 28:143–149. 10. Popovici RM, Lu M, Bhatia S, Faessen GH, Giaccia AJ, Giudice LC. Hypoxia regulates insulin-like growth factor-binding protein 1 in human fetal hepatocytes in primary culture: suggestive molecular mechanisms for in utero fetal growth restriction caused by uteroplacental insufficiency. J Clin Endocrinol Metab 2001; 86:2653–2659. 545
3303jum531-552onine_Layout 1 2/19/14 1:39 PM Page 546
Jerabek-Klestil et al—Prenatal Sonographic Diagnosis of Intrahepatic Portosystemic Shunts
11. Kocylowski R, Dubiel M, Gudmundsson S, Fritzer E, Kiserud T, von Kaisenberg C. Hepatic aminotransferases of normal and IUGR fetuses in cord blood at birth. Early Hum Dev 2012; 88:461–465. 12. Fisher C. A new vascular syndrome: the subclavian steal. N Engl J Med 1961; 265:912–913. 13. Hajdu J, Marton T, Kozsurek M, et al. Prenatal diagnosis of abnormal course of umbilical vein and absent ductus venosus: report of three cases. Fetal Diagn Ther 2008; 23:136–139. 14. Ferrero GB, Porta F, Biamino E, et al. Remittent hyperammonemia in congenital portosystemic shunt. Eur J Pediatr 2010; 169:369–372.
546
J Ultrasound Med 2014; 33:543–546
