Prenatal ultrasound risk factors for predicting postnatal heart failure in patients with congenital hepatic hemangiomas: a single-center study

Introduction

Congenital hepatic hemangiomas (CHHs) are localized vascular tumors that can develop in the fetal liver. Following superficial sites, the liver ranks as the second most prevalent site of congenital vascular tumors (1,2). CHHs are classified into 3 groups according to the clinical history and involution time: rapidly involuting congenital hemangioma (RICH), partially involuting congenital hemangioma (PICH), and noninvoluting congenital hemangioma (NICH). Most RICHs decrease in size by 80% at approximately 12 months of age; NICHs exhibit no postnatal regression and may grow proportionally with the patient; and PICHs show overlapping features and clinical behavior with RICHs and NICHs (3-5).

Patients with CHHs are usually asymptomatic in the prenatal period and are most often detected during routine prenatal examinations (6). Although patients with CHHs usually exhibit a favorable prognosis, some may experience complications and even death (7). Common complications include intralesional bleeding, anemia, thrombocytopenia, hypofibrinogenemia, and heart failure, among which heart failure is the most common cause of death (7,8). Several studies have shown that intrauterine therapy using a combination of corticosteroids and beta-blockers can be effective in inhibiting the growth of CHH and delaying the birth of the fetus (9,10). Therefore, the identification of reliable prognostic factors by prenatal imaging may help to identify which fetuses are the best candidates for prenatal intervention aimed at reducing the risk of infant morbidity and mortality.

Currently, ultrasonography, which allows for dynamic and multiangle visualization of lesion locations, is widely used for the prenatal diagnosis of CHHs (11,12). However, to our knowledge, there is limited research summarizing the prenatal ultrasound features of CHHs and their correlation with patient prognosis. Therefore, in this study, we aimed to identify prenatal ultrasound markers indicative of CHH combined with heart failure, thus offering imaging-based evidence for the prediction of patient outcomes and plan of early clinical intervention. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1596/rc).

Methods

Study population

Children diagnosed with CHH by prenatal ultrasonography and confirmed postnatally between January 2019 and December 2023 at our institution were included in this study. All CHHs were diagnosed according to the International Society for the Study of Vascular Anomalies (ISSVA) classification system (2). The diagnosis of CHH was established through a multimodal diagnostic approach incorporating clinical presentation, imaging characteristics, and histopathological confirmation when available. Study eligibility required fulfillment of both inclusion criteria: (I) definitive CHH diagnosis according to ISSVA classification guidelines, and (II) prenatal identification of hepatic mass lesions via standardized ultrasonographic protocols. Exclusion criteria were applied to cases demonstrating: (I) discordant histopathological or clinical features with CHH diagnostic criteria, or (II) incomplete medical records precluding comprehensive analysis.

The patients were categorized into an asymptomatic group and a group with concurrent heart failure based on their postnatal conditions. The asymptomatic group consisted of patients who did not present with intrauterine distress prenatally and did not present with clinical symptoms such as tachycardia, anemia, tumor rupture, and postnatal hemorrhage. In contrast, the group with concurrent heart failure included patients with CHHs who presented with dyspnea, cyanosis, cardiac enlargement, pulmonary hypertension, or cardiac insufficiency (13). This study was performed in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Shandong Provincial Hospital Affiliated to Shandong First Medical University (No. 2019-001). Informed consent was provided by all the patients’ guardians.

Prenatal and postnatal imaging evaluation

All prenatal ultrasound examinations were performed using the GE Voluson E10 (GE HealthCare, Zipf, Austria), Philips EPIC 7 (Philips Healthcare, Best, Netherlands), and Samsung W10 (Samsung Healthcare, Gangwon-do, South Korea) ultrasound diagnostic devices with an abdominal probe (3.5–5.0 MHz). During routine antenatal ultrasound screening, if a liver mass was detected, a comprehensive scan was conducted. The age of the pregnant women and the gestational age (GA) of the fetus at this time were recorded. On 2-dimensional (2D) ultrasound images, the location, size, boundaries, internal texture, and echogenicity of the mass and the fetal cardiothoracic ratio were determined. Color Doppler flow imaging (CDFI) was utilized to assess the vascular density, blood supply vessels, portal-systemic venous shunts (PSVSs), vascular dilation within the mass, and the presence of circulatory blood flow around the mass. In addition, fetal ductus-venosus blood flow spectra were measured to assess intrauterine fetal survival (14). Vessel path tracing: the course of feeding and draining vessels was meticulously traced using B-mode and Color Doppler to determine their anatomic origin (e.g., from the hepatic artery or portal vein) and drainage site (e.g., into a hepatic vein or directly into the inferior vena cava). Flow characterization: spectral Doppler was employed to distinguish between arterial and venous flow. Arterial supply was identified by high-velocity, pulsatile waveforms, whereas venous shunting was characterized by continuous, monophasic flow. To minimize errors, if there was any disagreement during the ultrasound examination, a senior physician was consulted to provide a diagnosis.

Postnatally, the prenatal imaging findings were confirmed in all patients. The initial confirmation was achieved through abdominal ultrasonography with Doppler. To clarify the characteristics and intervention plans, some children underwent magnetic resonance imaging (MRI) examinations after birth. Follow-up data included infant sex, treatment history, the incidence of tumor regression, and the incidence of complications.

Definition of sonographic parameters

The definitions of relevant tumor parameters were as follows (6,15-19). Fetal anemia was defined as middle cerebral artery peak systolic velocity (MCA-PSV) >1.5 Mom. Intrauterine fetal distress was defined when there was a decrease in MCA resistance to flow in late gestation [systolic/diastolic (velocity) ratio (S/D) <4.0] or when there was inversion or disappearance of the A-wave on venous catheterization and an increase in umbilical artery resistance to flow (S/D >3.0). Vascular density was assessed by counting the number of vessels within 1 cm² of the tumor in CDFI mode. Vascular density was categorized as low (<2 vessels/cm²), moderate (2–5 vessels/cm²), or high (>5 vessels/cm²). A venous lake was defined as an irregularly dilated vein within the tumor, with or without visible vascular walls (Figure 1A). A PSVS was defined as an abnormal connection between a branch of the portal vein and the hepatic vein within a tumor, identified by tracing the vessel course on 2D and Color Doppler imaging. Mixed color flow was observed prenatally by color Doppler ultrasound and identified postnatally by ultrasonography (Figure 1B). The presence of a hepatic arterial blood supply within the tumor was determined by color flow Doppler display of the arterial spectrum (pulsatile, high-velocity waveform) within the tumor (Figure 1C). Hepatic vein dilation was identified on ultrasound in the second hepatic portal section where the hepatic vein closest to the tumor had a wider diameter than the other hepatic veins (Figure 1D). Dilatation of the hepatic artery was defined as observation of a dilatated hepatic artery by 2D or color Doppler ultrasound during fetal life and confirmed by postnatal ultrasound (Figure 1E). The normal cardiothoracic area ratio is no greater than one-third (20).

Figure 1 Some typical sonographic features of images. (A) Venous lakes on a 2-dimensional ultrasound image (seen within calipers). The shape is irregular, and a fine, punctate, strong echogenic flow is seen within. (B) Portosystemic venous shunts are shown on CDFI (arrows). (C) The hepatic artery spectrum is seen in the blood supply vessels within the tumor. (D) The tumor was located in the right lobe of the liver, and CDFI revealed 2 adjacent hepatic veins that were significantly dilated compared to the LHV. (E) Dilated PHA. CDFI, color Doppler flow imaging; LHV, left hepatic vein; M, mass; MHV, middle hepatic vein; PHA, proper hepatic artery; RHV, right hepatic vein.

Statistical analysis

Qualitative data are presented as frequencies and percentages, and between-group comparisons were conducted using Fisher’s exact test. Alternatively, quantitative data are expressed as the median and quartiles, the between-group comparisons of which were performed using the nonparametric Mann-Whitney U test. Receiver operating characteristic (ROC) curve analyses were performed to determine optimal cutoff values for continuous variables. To explore the relationship between variables, Spearman correlation analysis was used. The significance level was derived from 2-tailed results and set at P<0.05. The data were analyzed using the software SPSS 25.0 (IBM Corp., Armonk, NY, USA).

Results

In total, 54 patients were enrolled in this study. None of the patients presented with intrauterine distress and the ultrasound spectrum of the ductus venosus flow showed A-wave positivity. All surviving children were followed up for more than 1 year, with the longest follow-up being more than 5 years after birth.

Among the included patients, 7 patients presented with concurrent heart failure (Table 1). All the symptoms in these children manifested within 1 month after birth: One patient died of multi-organ failure (MOF) due to heart failure after birth. A total of 4 patients received vascular embolization treatments, and 2 patients received steroid and propranolol therapy, which resulted in significant tumor shrinkage and the disappearance of clinical symptoms (Figure 2A-2D). Overall, 6 of the 47 asymptomatic cases demonstrated continued tumor enlargement in the first few months after delivery (excluding intratumoral bleeding) that gradually resolved over 3–6 months. At the last follow-up, complete regression was observed in 61.7% of the tumors, with minimal residual calcifications within some lesions (Figure 3A-3D). Partial regression was noted in 36.2% of the tumors, and one tumor showed no regression (Figure 4A-4B).

Figure 2 Images of a patient with postpartum combined heart failure. (A) A prenatal ultrasound image (gestational week: 36 W + 6 d) shows that the tumor is internally heterogeneous with several large venous lakes (arrows), and circumferential tubular echoes are visible in the outer posterior part of the tumor. (B) The 3-dimensional reconstruction shows abundant internal blood flow, an abnormal PSVS (arrows), and a circumferential blood flow envelope in the periphery of the lesion. (C) Ultrasonographic appearance of the mass after vascular embolization. Note the abundant hyperechogenic foci secondary to calcification. (D) There is a decrease in the amount of color Doppler flow along the peripheral margins of the lesion. M, mass; PSVS, portal-systemic venous shunt.

Figure 3 Ultrasonographic images showing progressive tumor involution in a case of asymptomatic RICH presenting during late pregnancy. The markers on (A-C) are superimposed on the tumor. (A) At presentation during the prenatal period (37 W + 2 d), a tumor with mixed moderate echoes, clear hyperechoic periphery, and peripheral blood flow measuring 6.5 cm × 3.3 cm × 5.2 cm was identified in the right hepatic lobe. (B) In the immediate neonatal period, a similar tumor appearance and size were noted. (C) At 1 month of age, the tumor measured 5.4 cm × 4.9 cm × 4.5 cm and demonstrated coarse hyperechogenic foci consistent with internal calcifications. (D) At 9 months of age, the tumor decreased significantly in size and was seen primarily as a cluster of calcifications. RICH, rapidly involuting congenital hemangioma.

Figure 4 Prenatal and postnatal ultrasonographic images of a NICH (white markers). (A) The mass was hypoechoic prenatally (34 W, 0.7 cm × 0.8 cm) when compared to the adjacent liver parenchyma. (B) The mass was hyperechoic postnatally (1.4 cm × 1.1 cm) when compared to the adjacent liver parenchyma. NICH, noninvoluting congenital hemangioma.

The mean age of the pregnant women included in this study was 30 years (20–43 years), with a median gestational week at initial detection of 34 W⁺ (18 W⁺³ to 40 W⁺²); 92.59% of the lesions were detected in the late stages of pregnancy. Among the 54 patients, all CHHs were focal, with 51.9% of the lesions located in the right lobe of the liver. In 98.15% of the patients, the tumor boundaries were clear. Approximately 94.4% of the tumors showed a visible circulatory or semicirculatory blood flow pattern at the periphery, and 92.6% displayed a moderate or high vascular density within the tumor. All tumors had blood supplied by vessels connected to the portal vein.

According to the ultrasound images obtained upon initial diagnosis, 10 patients had a concurrent hepatic arterial blood supply, comprising 4 patients (57.1%) in the concurrent heart failure group and 6 patients (12.8%) in the asymptomatic group (P=0.0017). The median maximum tumor diameter in the concurrent heart failure group was 6.5 cm, which was significantly greater than that in the asymptomatic group (3.8 cm; P=0.001). Patients in the concurrent heart failure group had an increased cardiothoracic ratio, in contrast to those in the asymptomatic group, who had a ratio within the normal range (P<0.001). Hepatic vein dilation was observed in 55.6% (30/54) of the patients, including 7 patients in the concurrent heart failure group and 23 patients in the asymptomatic group (P=0.013). Among the 24 patients with hepatic artery dilation, 7 were in the concurrent heart failure group, and 17 were in the asymptomatic group (P=0.002). PSVSs were detected in 16 patients: 7 in the concurrent heart failure group and 9 in the asymptomatic group (P<0.001). Venous lakes were observed in 22.2% (12/54) of the patients: 7 and 5 patients in the heart failure and asymptomatic groups, respectively (P<0.001) (Table 2). In addition, ROC analysis showed that the area under the curve (AUC) for initial tumor diameter to predict concomitant heart failure was 0.859, with an optimal cutoff value of 4.85 cm, at which point the sensitivity was 100% and the specificity was 70.2%.

Correlation analyses were also conducted to explore the relationships between factors that exhibited pairwise differences between the 2 groups. Results revealed that PSVSs were associated with hepatic artery dilation (P=0.001), venous lakes (P<0.001), and hepatic vein dilation (P=0.003). Moreover, hepatic artery dilation exhibited significant correlations with the hepatic artery blood supply (P=0.003), venous lakes (P=0.022), and hepatic vein dilation (P=0.014) (Table 3).

Discussion

This study revealed that CHHs are typically observed in late pregnancy by prenatal ultrasound imaging. The lesions typically appear as solitary entities with clearly defined borders. They predominantly exhibit uneven, low internal echogenicity, have tortuous and dilated vascular patterns, and may occasionally show calcifications. The blood flow signals within the tumors are generally rich, indicating portal vein supply and hepatic venous reflux, with peripheral vessels forming a ring or semi-ring shape. The presence of an increased cardiothoracic ratio, hepatic vascular dilation, abnormal tumor enlargement, hepatic artery blood supply, PSVSs, and internal echogenicity with venous lakes during an initial prenatal ultrasound examination may indicate an elevated risk of postnatal heart failure in fetuses with CHHs.

In contrast to infantile hemangiomas, which predominantly affect females, the CHHs showed a nearly 1:1 sex ratio in this study, consistent with previous findings (1,21). Unlike previous studies (22) that indicated a greater incidence of CHHs in the right lobe of the liver, this study revealed a nearly equal tumor location distribution between the left and right lobes (26:28), possibly owing to the larger sample size.

All patients who developed congestive heart failure (CHF) exhibited prenatal ultrasound evidence of PSVSs within the tumor. Additionally, correlations between the presence of PSVSs and the presence of venous lakes, hepatic artery dilation, and hepatic vein dilation were identified. Therefore, we hypothesize that PSVSs may lead to the direct passage of portal venous blood into veins through abnormal communication, thereby increasing venous blood flow within these tumors. This, in turn, could enhance the likelihood of venous dilation and the formation of venous lakes. Moreover, a positive correlation was noted between the severity of PSVSs and an enlarged size and a greater frequency of venous lakes within the tumor. Venous lakes were consistently present in patients who later developed CHF, which is consistent with the findings of Waelti et al. (16), who associated venous lakes with heart failure. Although venous lakes were present in 5 patients in the asymptomatic group, they were characterized by their relatively small size and primarily occurred as solitary entities. Shunting increased venous blood reflux within the tumor, thereby increasing the likelihood of dilation in nearby hepatic veins. Additionally, shunting reduced the supply of oxygen-rich blood to the liver, triggering compensatory arterial supply and potential arterial dilation. Severe PSVS results in increased cardiac output, which may eventually lead to an increased cardiothoracic ratio and high-output CHF. This finding aligns with previous literature reports and theories on the dual blood supply system of the liver (4,13,23,24). Additionally, the Francophone Society of Pediatric and Perinatal Imaging—Fetal Imaging Radiopediatric Research Group (6) previously conducted a portal-systemic shunt procedure in a patient with CHH who was 30 days old using PSVSs, leading to effective postoperative relief of heart failure and pulmonary arterial hypertension. This finding supports our inference. Additionally, in our study, all patients with concomitant CHF presented after birth. This may be associated with the favorable preservation of fetal circulation due to elevated pulmonary arterial pressure during fetal life (17).

All patients demonstrated a tumor blood supply from the portal vein. This may be because the primary blood supply of the liver originates from the portal vein. During fetal development, oxygenated blood in the placenta is delivered to the portal vein (70–80%) and ductus venosus (20–30%) through the umbilical vein (25). Some participants exhibited a simultaneous blood supply from both the portal vein and the hepatic artery, which was more prevalent in the group with concurrent heart failure. Therefore, the presence of a hepatic arterial blood supply within these tumors may increase the risk of heart failure in children and constitutes a partial explanation for hepatic artery dilation. Elevated cardiac output may also contribute to hepatic artery dilation.

Notably, in this study, the simultaneous occurrence of a hepatic artery supply and PSVSs within the tumors strongly suggested concomitant heart failure. We hypothesize that hepatic arterial supply within the tumor may be an independent risk factor for concomitant heart failure. In addition, hepatic vessel dilation, the presence of venous lakes, and an elevated cardiothoracic ratio are considered compensatory or decompensatory manifestations caused by PSVS.

In the present study, a significant difference in maximum tumor diameter was observed between the 2 groups, which is consistent with previous studies (8,22,26). Moreover, in this study, the risk of complicated heart failure was elevated when the initial tumor diameter exceeded 4.85 cm, as shown by ROC analysis.

Few studies have reported the pathological manifestations of CHHs (5). Similarly, in this study, pathological results were obtained from only 1 patient who died 2 days after birth due to heart failure. The pathological presentation closely aligned with the ultrasound description of the tumor, featuring a primarily hypoechoic appearance with a well-defined border and strong echogenic edges (Figure 5A-5C). The internal echogenicity displayed nonuniformity, with several venous lakes manifesting as hypoechoic areas.

Figure 5 Images of a liver mass in a patient who died of MOF on day 2 of life. (A) Prenatal ultrasound image (35 W). The tumor measured 6.5 cm × 6.3 cm × 5.3 cm, with venous lakes indicated by the white arrow. (B) Postnatal macroscopic image of the gross specimen shows an irregular mass with a visible peripheral peritoneum. Several cysts are seen in the center of the mass, containing slightly turbid fluid, surrounded by a dark red, solid, soft-textured mass (white arrows). (C) The microscopic image of the specimen shows that the interior of the mass consisted of a large number of proliferating vascular endothelial cells, with lumens of varying sizes, predominantly thin-walled small blood vessels, and residual small bile ducts between the lumens (H&E stained; magnification ×200). MOF, multi-organ failure.

This study has some limitations. First, the results might have been influenced by the relatively small sample size. Therefore, we will continue to collect further relevant data from new eligible participants to increase the sample size and statistical power of this study. However, given the rarity of CHHs in fetuses, this study is the largest prospective case-control study on the subject to date. Second, only 1 patient underwent pathological examination. However, this did not impede our ability to diagnose this condition. Clinical treatment guidelines specify that CHHs occurring during fetal development can be diagnosed using clinical outcomes and imaging examinations, and pathological examination is typically deemed unnecessary (7).

Conclusions

The findings of this study indicate an elevated risk of postnatal CHF in infants when the prenatal ultrasound indicates CHH with sonographic features such as a tumor diameter exceeding 4.85 cm and the presence of a hepatic artery supply or PSVS. Furthermore, PSVS and hepatic artery supply may be key factors contributing to heart failure. For these patients, monitoring during the perinatal period should be enhanced, delivery should take place in tertiary hospitals, and early intervention should be implemented as needed to reduce mortality and improve the overall prognosis. To this end, future prospective studies are warranted to validate these prenatal predictors of postnatal heart failure.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1596/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1596/dss

Funding: This work was supported by the National Natural Science Foundation of China (No. 82302149 to T.G.), the Natural Science Foundation of Shandong Province (No. ZR2020QH267 to T.G.), China Postdoctoral Science Foundation (No. 2022M711987 to T.G.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1596/coif). All authors report this research was supported by the National Natural Science Foundation of China (No. 82302149), the Natural Science Foundation of Shandong Province (No. ZR2020QH267), and the China Postdoctoral Science Foundation (No. 2022M711987). L.L. is from Philips Healthcare. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was performed in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Shandong Provincial Hospital Affiliated to Shandong First Medical University (approval No. 2019-001). Informed consent was taken from all the patients’ guardians.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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