The abnormal course of the umbilical vein (UV), and the absence and displacement of the portal vein (PV) or the ductus venosus (DV) in the fetus can cause shunting into the systemic veins. This rare anomaly has recently been re-classified under the term ‘umbilical-portal-systemic venous shunts’ (UPSVS). Based on the anatomical origin of the shunt (umbilical, portal, or ductal), UPSVS is classified into 3 types: Type I, umbilical-systemic shunt (USS); Type II, ductus venosus-systemic shunt (DVSS); and Type III, portal-systemic shunt which is further divided into 2 subtypes: Type IIIa, intrahepatic portal-systemic shunt (IHPSS) and Type IIIb, extrahepatic portal-systemic shunt (EHPSS). Distinct from previously used postnatal dichotomous classification, that is, intra- and extrahepatic shunts,[3–8] the new classification takes into account the unique anatomy of the fetus, that is, the umbilical, portal and DV form a functionally inseparable system, in which each component (UV, PV, or DV) can produce a shunt with systemic veins. Therefore, the new classification system is believed to be more suitable for prenatal analysis of the clinical and prognostic characteristics of UPSVS. According to the new classification, the absence of a normal DV does not stand alone as a pathology, although a number of studies have described prenatal diagnosis of DV agenesis.[9–16]
To date, there has been scarce documentation about prenatal diagnosis of UPSVS, warranting further studies to expand our knowledge to improve perinatal outcome prediction and management.[1,2] There are few case reports that have focused on the prenatal analysis of UPSVS but have used the postnatal dichotomous classification.[17,18] Since its establishment, the new classification has not been applied to the prenatal analysis of UPSVS. Here, we retrospectively analyzed UPSVS cases identified from a large cohort of fetuses (>60,000) and presented the prenatal sonographic characteristics, birth outcomes, and follow-up results of UPSVS following the new classification system.
This study was approved by the Research Ethics Committee of Qilu Hospital of Shandong University, and the Medical Research Ethics Committee of the Affiliated Hospital of Jining Medical University with the waiver of the requirement for obtaining informed consent due to the nature of the retrospective study. Fetal sonograms taken from April 2016 to July 2018 at the Department of Ultrasound, Qilu Hospital of Shandong University and the Department of Ultrasound, the Affiliated Hospital of Jining Medical University were retrospectively reviewed. Additionally, clinical data and follow-up results of those with UPSVS were analyzed.
Pregnant women undergoing regular ultrasound monitoring received the standard 2D procedure using the Philips iU22 ultrasound system with a 3.5 to 5.0 MHz transducer. This included transabdominal scanning to examine the fetus, the placenta and amniotic fluid, and sagittal scanning to visualize the ductus venosus. In the case of suspected anomaly, a further 3-plane scan of the fetal venous system was carried out as described by Yagel et al:
- a transverse abdominal plane scan was done at the level of left portal sinus to examine the umbilical vein (UV), left portal vein, portal sinus, anterior right portal vein, posterior right portal vein, main portal vein, and splenic vein and artery;
- moving the transducer cephalad, a ventral or lateral transverse plane was used to image the right, middle and left hepatic veins and inferior vena cava (IVC);
- longitudinal anteroposterior plane scanning was performed to image the UV, ductus venosus, IVC and left hepatic vein. Pulsed-wave Doppler imaging of a given target vessel was performed in all cases of UPSVS. Postnatal follow-ups were conducted up to 1 year.
A total of 61,082 fetal sonograms were retrospectively reviewed. Ten cases of UPSVS were identified, which included 4 cases of USS (cases 1–4); 3 cases of DVSS (case 5–7) and 3 cases of IHPSS (cases 8–10). Cases 8 and 9 were referred to our department for a suspected UPSVS. Post-birth follow-ups ranged from 3 to 12 months. Characteristics and outcomes of all cases are shown in Table 1.
The UV was found to drain into the IVC in all Type I UPSVS cases, and there was complete absence of DV and intrahepatic portal venous system, shown in the sonogram of case 2 in Figure 1. Two cases of USS had trisomy 21. Displacement of the splenic vein and the superior mesenteric vein were detected in cases 1 and 2, respectively, which resulted in drainage into the UV. Pulsed-wave Doppler examinations showed triphasic waveforms at the shunt site in all 4 cases of USS (Fig. 1, inserted). Pregnancy was terminated in all Type I shunt cases.
In the new classification system, the Type II shunt is defined as a short DV connecting to the IVC below the pre-diaphragmatic infundibulum or a short DV draining into the hepatic vein with an intact UV–PV–DV structure. In case 5, the UV, PV, and DV were seen; however, the DV was found to connect to the hepatic fragment of the IVC (Fig. 2), and DV type velocity waveforms were detected at the shunt site (Fig. 2, inserted). The PV and its branches were visible and appeared normal, indicating an intact intrahepatic portal venous system (images not shown). Full-term birth took place in case 5 and no abnormalities up to 1-year postnatal follow-up were observed. Case 6 had persistent left superior vena cava and C-section was performed at 37 weeks; the infant was healthy at 4-month follow-up. Ultrasound examination was declined in cases 5 and 6 during follow-ups. One case of DVSS had trisomy 21 and the pregnancy was terminated as requested by the family (Table 1).
A shunt between the inferior branch of the left portal vein and the left hepatic vein was detected in Case 8 (Fig. 3). Additionally, turbulent blood flow and an enlarged left hepatic vein were detected at the shunt site (Fig. 3). The baby was born full term with hypoglycemia that disappeared 1 month after birth. Case 9 had multiple left/middle hepatic/portal vein shunts (Fig. 4) with a karyotype of 46, XY, inv (9) (p12q13); the baby was born full term with jaundice and abnormal liver function. The baby was hospitalized for 1 month and recovered. Typical triphasic waveforms were detected at the shunt site of the left portal vein of cases 8 and 9 (Figs. 3 and 4, inserted, respectively). Case 10 had a shunt between the inferior branch of the left portal vein and middle hepatic vein, the baby was born full term and surgery was performed 12-days post birth to repair the shunt. Intrauterine growth restriction was observed in all cases of Type IIIa UPSVS. The portal-hepatic venous shunt in cases 8 and 9 was not closed at the 6-month follow-up as shown by sonography examination. The 3-month follow-up of case 10 showed that the infant was healthy.
Prenatal studies of UPSVS in large series have rarely been reported, and the prevalence of fetal UPSVS remains unknown. We identified 10 cases of UPSVS in 61,082 fetuses, representing a prevalence rate of 1.64 per 10,000 fetuses. Considering that cases 8 and 9 were referred to our department, the UPSVS prevalence could be even lower. Ono et al screened 293,416 neonates and found that 8 had intrahepatic portal-systemic shunts and 3 extrahepatic portal-systemic shunts. This postnatal finding, together with our results, suggest that UPSVS is rare.
Following the new classification, we discovered that fetuses with Type I shunts had the poorest prognosis, that is, pregnancy termination in all 4 cases. The worst outcome for USS, that is, lowest rates of live birth and postnatal survival, was also observed in a previous study. In all Type I cases we examined, complete absence of intrahepatic portal venous system was noted, which is the determining factor for the termination of pregnancy. Additionally, we found that 2 Type I, 1 Type II and 1 Type IIIa UPSVS cases had abnormal karyotypes (Table 1). Volpe et al also revealed chromosomal abnormality (1/3) in Type I shunts (UV connection to the iliac vein). In contrast, Achiron and Kivilevitch revealed no chromosomal abnormalities in Type I (0/7) or Type III (0/16) shunts, but in Type 2 shunts (4/19). Weissmann–Brenner and Zalel karyotyped 5 of 6 fetuses with UV drainage into the IVC and reported that 4 had chromosomal abnormalities, including trisomy 21, trisomy 13, etc. These authors did not provide information about the PV and hepatic veins, but reported DV agenesis in all 5 cases, indicating the shunts are not Type II. Chromosomal abnormalities in DV agenesis (non-Type II) cases were reported at a prevalence of 20.2% (24/119). Taken together, we concluded that chromosomal abnormalities could occur in any of the 3 types of shunts. We also observed choroid plexus cysts in case 1, cardiomegaly in case 2, and ventricular septal defect and nasal bone agenesis in case 3. These results are in agreement with previous reports showing that USS is associated with a high occurrence of other organ anomalies.[2,21]
Case 5 had a satisfying outcome, mainly due to the presence of the intrahepatic portal venous system. A high incidence of chromosomal abnormalities among Type II shunts was reported. We found 1 case of Type II with trisomy 21 (case 7). It has been shown that fetuses with IHPSS have the highest rate of live birth compared with those with other types of shunts. In our series, full-term birth took place in all cases of IHPSS. A common postnatal problem associated with IHPSS is the abnormal liver function that was observed in case 9. Han et al conducted a follow-up study of 6 neonates with intrahepatic portosystemic venous shunts and found 5 who spontaneously closed at approximately 1 year. Cases 8 and 9 did not display shunt closure at 6 months post birth, probably due to the short follow-up time. No EHPSS cases were identified in this study. Of note, the presence of intrahepatic portal venous system in EHPSS is of paramount importance for the best outcome. UPSVS is rare, and from over 60,000 sonograms, we only identified 10 cases of UPSVS. This small sample size is a limitation of this study. Nevertheless, the information gathered from these cases under the new classification of UPSVS is valuable, for example, chromosomal abnormalities, and other organ anomalies were observed in all 3 types of UPSVS, which can be used to predict fetal outcomes and direct perinatal management.
UPSVS is extremely rare. Fetuses with Type I shunts have the poorest prognosis and the presence of the intrahepatic portal venous system is key to live birth regardless of UPSVS types. Chromosomal abnormalities and other organ anomalies can occur in any types of UPSVS. Therefore, karyotyping and examinations of other organs should be performed once UPSVS is detected. To our knowledge, this is the first study to apply the new UPSVS classification, since its establishment, to investigate the clinical and prognostic characteristics of UPSVS. Our results suggest prenatal analysis with the new classification system is helpful in predicting the fetal outcomes and directing perinatal management.
We sincerely thank Mr. Anthony Cannavicci from the University of Toronto for help in English editing.
Conceptualization: Guowei Tao.
Data curation: Haifang Wu and Zhonglu Zhang.
Formal analysis: Haifang Wu and Zhonglu Zhang.
Funding acquisition: Guowei Tao and Zhe Ma.
Investigation: Haifang Wu, Guowei Tao, Qi Li, and Zhonglu Zhang.
Methodology: Guowei Tao.
Project administration: Zhe Ma.
Software: Qi Li.
Supervision: Xiang Cong and Jing Zhang.
Validation: Xiang Cong.
Visualization: Haifang Wu, Guowei Tao, Jing Zhang, and Zhonglu Zhang.
Writing – original draft: Haifang Wu.
Writing – review & editing: Guowei Tao.
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Keywords:Copyright © 2019 The Authors. Published by Wolters Kluwer Health, Inc. All rights reserved.
chromosome abnormality; prenatal; ultrasonography examination; umbilical-portal-systemic venous shunt