Background
The early diagnosis of cholestasis in newborns, when caused by true liver disease and not physiological or transient jaundice is usually eluded. Across North America and Europe, the commonest causes of cholestasis are fibroinflammatory cholangiopathy and biliary atresia [1].
The inflammatory and fibrotic obliteration of the hepatic biliary ducts affects the normal drainage of bile and causes biliary atresia (BA) which presents with neonatal and infantile persistent jaundice. If left untreated, it necessarily progresses to hepatic cirrhosis and consequent failure, leading to inevitable death within the first 2 years of life. Patients with biliary atresia and those with other cholestatic liver disease overlap in their clinical presentation and blood biochemistry representing a great challenge to clinicians in early and accurate diagnosis. Early biliary-enteric diversion through the Kasai portoenterostomy procedure helps restore bile flow and avoid rapid progression to biliary cirrhosis. Hence, early diagnosis of BA is of great importance for proper surgical selection and planning [2].
Other available diagnostic techniques as nuclear medicine studies HIDA (hepatoiminodiacetic acid) scan, cases of biliary atresia show no tracer activities in the intestines after 24 h. The accuracy of HIDA scan were different by the maturity of the patient, age at testing and severity of cholestasis. However, The sensitivity and NPV were 91.2 and 85.3% while specificity and PPV were 80.6 and 88.1%. These results suggested that HIDA is suboptimal in both diagnosing or excluding BA [3].
Cirrhosis is a serious and rapid complication of biliary atresia, the gold standard diagnosis of fibrosis is by biopsy which is considered an invasive procedure with various adverse effects. The available noninvasive techniques for measuring liver fibrosis are poorly developed and inconclusive in children including biochemical tests such as APRI (aspartate transaminase-to-platelet ratio index). Having these considerations in mind, it is of utmost importance to develop noninvasive methods to evaluate liver stiffness and hence expedite the diagnosis of biliary atresia and consequently the timing of the Kasai operation [4].
Abdominal ultrasound (US), a widely available and non-invasive diagnostic tool is considered to be the first-line imaging modality in the assessment of children with diffuse liver disease [5]. Ultra sonographic features suggestive in diagnosing BA include; the abnormal gallbladder morphology and triangular cord (TC) sign. However, the reliability of these signs is rather controversial owing to the lower sensitivity of the TC sign in patients with early-stage BA and the fact that an under-distended or partly collapsed gallbladder could also present in non-BA patients; thus, in a suspected case of BA, it is impractical to rely on conventional US alone to have a confident diagnosis. To maximize the diagnostic reliability of US as an initial imaging modality to diagnose BA ultrasound elastography has been introduced as a quantitative non-invasive sonographic technique to measure liver stiffness which is presumed to be different in BA from other cholestasis [1].
Post-Kasi disease progression is usually assessed by the assortment of laboratory and radiologic testing with a careful contemplation of the need for repeated liver biopsy and/or upper gastrointestinal endoscopy, both being invasive with procedural as well as anesthesia-related risks. To date, there are no available standardized guidelines for non-invasive staging of hepatic fibrosis nor timing for endoscopic evaluation for the follow-up of patients which led to the need to properly investigate the utility of SWE in both early diagnosis of BA as well as post-Kasi follow-up [6].
This study aims to investigate Shear Wave Elastography's accuracy in assessing pediatric cholestasis and differentiating biliary atresia from other causes.
Patients and methods
Study population
(This study is a case control analytical study) The study enrolled 59 pediatric patients with cholestatic liver disease (increased bilirubin more than 2 mg/dl) and 21 matching controls with normal liver function tests.
The study population is categorized into three groups:
Group A (n = 30): with cholestasis due to biliary atresia (BA), underwent liver biopsy 20 patients were followed by post-Kasai portoentrostomy (HPE), then 3 months follow-up after the Kasai (HPE) operation whereas 10 patients of this group were not followed up (either died or were not accessible)
Group B (n = 29): non-biliary atresia-related cholestasis (5 underwent liver biopsy).
Group C (n = 21): age and sex-matched control.
We excluded those with Contraindication of liver biopsy, abnormal coagulation profile, and thrombocytopenia as well as clinically unstable patients and Patients with marked ascites.
Methods
Clinical examination:
Full history taking and Clinical examination including the presence of fever, jaundice, and stool color.
Laboratory investigations
Liver function tests: Aspartate transaminase (AST), Alanine transaminase (ALT), Alkaline phosphatase (ALP), bilirubin (total and direct), Gamma-glutamyl transferase (GGT), albumin, prothrombin time (PT), INR, and Complete blood count (CBC).
APRI score is calculated (aspartate aminotransferase to platelet ratio index)
B-mode US and SWE examination
We used a Sony (Aplio 400, Japan) brand device to perform B-mode US and SWE in all patients and volunteers performed by WA Elzayat with 18 years of experience in pediatric radiology. The application applied was Acoustic Radiation Force Impulse (ARFI) imaging-based SWE implementing a virtual touch tissue imaging quantification (VTIQ) option. Subjects were examined in the supine or slight left lateral position with the arm raised above the head to increase the intercostal space in full inspiratory phase.
The liver dimensions, echogenicity, degree of heterogeneity, and biliary system dilatation were examined in B-mode, and then 2D-SWE software was activated in split-screen mode. Measurements were taken in the right lobe of the liver through an intercostal space at the intersection of the mid-axillary line and a transverse line at the xiphoid process level with the transducer perpendicular to the liver capsule. Ten measurements were taken 1.5 to 2 cm below the liver capsule using a 3 mm in diameter round-shaped ROI in full inspiratory phase. When choosing the region of interest position we tried to avoid large blood vessels and bile ducts. The unit of measurement recording was m/s. The mean stiffness value for the right lobe was calculated by averaging the ten measurements.
Liver biopsy
1 h before the biopsy baseline vital signs were recorded, including the heart rate (HR), arterial blood pressure (BP), respiratory rate (RR), and core body temperature.
Needle liver biopsy technique using aspiration or suction (Menghini). The needle bore ranged from 1.6 to 1.8 mm in internal diameter and a needle length of 7–9 cm, depending on the patient’s age.
The needle was introduced in the right mid-axillary line above the rib, just one intercostal space below the maximum liver dullness under local infiltration anesthesia by lidocaine hydrochloride.
The biopsies were fixed in 10% formol saline and stained using hematoxylin and eosin.
Post biopsy: Patients were placed in the right lateral decubitus and were asked to fast for at least 4 h after the biopsy. Vital signs (HR, RR, BP, and temperature) were monitored and recorded regularly, every half an hour for the first 2 h and every hour next 2 h.
Follow-up of patients
Patients were followed up 3 months post-operative.
Radiological evaluation: liver size, texture, and SWE–Laboratory investigations; (AST), (ALT), bilirubin (total and direct), GGT, albumin and prothrombin time (PT), INR, and complete blood count (CBC) were done.
The success of the Kasai operation was determined by the restoration of bile flow with a coloration of stools (Bilirubin less than 2 gm/dl).
Statistical analysis
The chi-square test or Fisher’s exact test was used as appropriate. For numeric data, the Mann-Whitney U test was performed to compare biliary and non-biliary atresia groups. Kruskal-Wallis test was used to compare biliary, non-biliary, and control groups. Bonferroni adjusted pairwise comparisons were performed for the statistically significant variables with more than two categories. The diagnostic accuracy (sensitivity and specificity) of SWE were calculated as well as positive predictive value (PPV), negative predictive values (NPV), and overall accuracy. Receiver Operator Characteristic (ROC) analysis was used to determine the diagnostic discrimination of SWE in predicting the type of atresia, and the state post-Kasai procedure was performed. The area measures accuracy under the ROC curve (AUC). An area close to 1.0 represents a perfect test; an area close to 0.5 represents a worthless test. All tests were 2-tailed, P values less than 0.05 were considered statistically significant, and a 95% confidence level was used.
Results
Demographics and clinical characteristics
The age was significantly decreased among the biliary atresia group than in the non-biliary atresia group (P < 0.001). Also, the yellow stool was the most common among the biliary atresia and non-biliary atresia group (P = 0.034). On the other hand, there were no significant differences among the studied groups regarding gender and jaundice.
In group B (Non-biliary atresia patients), ten (34.48%) were diagnosed with cholestasis, with normal or low GGT levels. Five patients (17.24%) were diagnosed with hepatitis, and 3 patients had syndromes (10.34%) (2 patients had Arthrogryposis-renal dysfunction-cholestasis and 1 patient had Allagile). Other causes were found in 11 patients (37.93%) including Criger-Najar (n = 4), choledochal cyst (n = 3), bile acid synthetic defect (n = 2), Dubin Jonson (n = 1) and idiopathic causes (n = 1).
Platelets were significantly decreased among the biliary atresia group than in the non-biliary atresia group (P = 0.024). While direct bilirubin, GGT, and aminotransferase platelet ratio index were significantly higher among the biliary atresia group than in the non-biliary atresia group (P < 0.05).
On the other hand, there were no significant differences among the studied groups regarding total leukocyte count, hemoglobin, bilirubin, alanine aminotransferase, aspartate transaminase, alkaline phosphatase, albumin, and prothrombin time/control (P > 0.05)
Biopsy results
In Group A (Biliary atresia patients), a major bile duct obstruction with fibrosis/cirrhosis was found, with most having mild fibrosis (40%), followed by moderate (36.67%), marked fibrosis (13.33%), and secondary cirrhosis (10%). A statistically significant relationship was found between the degree of fibrosis and the APRI score (p = 0.048) (Fig. 1). Patients with secondary biliary cirrhosis had a higher APRI score (6.45 ± 5.83) than those with other fibrosis grades.
Fig. 1 [Images not available. See PDF.]
Biopsy results (degree of fibrosis) in relation to APRI score
Five non-biliary atresia patients (group B) had biopsy results (17.25%), 2 patients (6.90) had neonatal giant cell hepatitis, 2 patients (6.90%) had a paucity of the interlobular bile ducts, one patient (3.45%) had chronic hepatitis with mild activity and fibrosis.
SWE
Mean shear wave elastography was significantly higher among the biliary atresia group (median 2.32) than in non-biliary atresia (median 1.74) and control groups (median 1.64) (P < 0.001) (Table 1).
Table 1. Mean SWE among biliary, non-biliary atresia, and healthy controls (N = 80)
Variable | Non-biliary atresia (N = 29) | Biliary atresia (N = 30) | Healthy controls (N = 21) | P value |
|---|---|---|---|---|
Mean SWE | 1.74 (1.35–2.80) 2.02 ± 0.96 | 2.32 (1.61–5.90) 2.85 ± 0.75 | 1.64 (1.42–1.90) 1.70 ± 0.95 | < 0.001* |
Median (Range) | ||||
Mean±SD | ||||
Posthock test | P1 < 0.001*, P2 = 0.447, P3P1 < 0.001* | |||
SWE: Shear wave elastography. P1: compared non-biliary atresia vs. biliary atresia. P2: compared non-biliary atresia vs. healthy controls. P1: compared biliary atresia vs. healthy controls
There was a statistically significant relationship between the degree of fibrosis and the SWE score (p = 0.002). Patients with marked fibrosis had higher SWE scores (3.83 ± 1.17), followed by secondary biliary cirrhosis (3.37 ± 1.75), then moderate fibrosis (2.01 ± 0.30), then mild fibrosis (1.95 ± 0.31) (Table 2).
Table 2. Biopsy results (degree of fibrosis) in relation to SWE value
Biopsy results | SWE value | 95%CI | F | P value | ||
|---|---|---|---|---|---|---|
Mean ± SD | Range | Lower bound | Upper bound | |||
Major bile duct obstruction: | 5.183 | 0.002* | ||||
Marked fibrosis | 3.83 ± 1.17 | 1.99–5.90 | 3.08 | 4.58 | ||
Moderate fibrosis | 2.01 ± 0.30 | 1.61–2.43 | 1.80 | 2.23 | ||
Mild fibrosis | 1.95 ± 0.31 | 1.68–2.31 | 1.16 | 2.74 | ||
Secondary biliary cirrhosis | 3.37 ± 1.75 | 1.91–5.32 | −0.984 | 7.73 | ||
SWE: Shear wave elastography. F: ANOVA F test. *Significant.
ROC curve analysis was performed to assess the diagnostic performance of US SWE measuring and discriminating patients with or without biliary atresia; the best cutoff value for SWE = 1.97 with a sensitivity of 75.0% and specificity of 83.5%, area under the curve of 0.819 (95% CI = 0.699–0.937) for predicting the type of atresia (biliary/non-biliary) with positive and negative predictive value were 82.8% and 74.1%, respectively Fig. 2.
Fig. 2 [Images not available. See PDF.]
ROC curve analysis for prediction of biliary atresia using SWE (Shear wave elastography) in pediatric patients (n = 59), p value < 0.001
Post-Kasi
Direct bilirubin was significantly decreased post-Kasai state (4.35 ± 4.19) compared to the Pre-Kasai state (8.19 ± 3.10), (P = 0.001). While, other investigations as total leukocyte count, hemoglobin, platelet, total bilirubin, alanine aminotransferase, aspartate transaminase, arterial pressure, gamma-glutamyl transpeptidase, albumin, prothrombin time did not show any significant difference between pre and post kasai results (P > 0.05).
The mean shear wave elastography didn't show any significant difference among succeeded (n = 17) (Fig. 3) and failed groups (P = 0.67). N = 3 (Fig. 4 and Table 3).
Fig. 3 [Images not available. See PDF.]
Two-month-old female patient presented with jaundice: total bilirubin, 8 mg/dl, direct bilirubin, 5.1 mg/dl, and GGT, 1209 u/l. Greyscale US showed an average liver size with homogenous echotexture. A liver biopsy revealed major bile duct obstruction (extrahepatic biliary atresia) with moderate fibrosis. a and b SWE measurements at the right hepatic lobe showing homogenous color-coded SWE. The mean SWE value was 1.78 m/sec. c and d Follow-up in 3 months showed successful Kasai operation; mean SWE value in the right hepatic lobe was 1.61 m/sec)
Fig. 4 [Images not available. See PDF.]
Two-month-old male patient presented with jaundice: total bilirubin, 11.4 mg/dl, direct bilirubin, 7.9 mg/dl, and GGT, 840 u/l. Greyscale US revealed mild hepatomegaly with heterogeneous echotexture. Liver biopsy revealed major bile duct obstruction (extrahepatic biliary atresia) with marked fibrosis (impending cirrhosis). Follow-up period of 3 months showed failed Kasai operation and pending liver transplantation. a and b SWE measurements at the right hepatic lobe showing heterogeneous color-coded SWE. The mean SWE value was 5.42 m/sec
Table 3. Follow up state post-Kasai procedure in relation to SWE (N = 20)
Post-Kasai procedure state (N = 20) | |||
|---|---|---|---|
Variable | Succeeded N = 17 | Failed N = 3 | P value |
Mean SWE | 3.30 (2.13) (1.45–5.75) | 3.63 (1.70) (2.39–4.39) | 0.973 |
Median (IQR) | |||
Range | |||
Regarding the diagnostic accuracy of SWE in predicting outcomes in post-Kasai patients we found the best cutoff value of SWE for predicting outcomes in post-Kasai procedure to be 3.55, with a sensitivity of 66.7%, specificity of 64.7%, area under the curve 0.510 (95% CI = 0.184–0.836), positive and negative predictive values were 25% and 91.7% respectively, with accuracy 65%.
Discussion
We enrolled 39 patients with biliary atresia, 29 patients with non-biliary atresia-related cholestasis, and 21 matching controls. Our study showed that the biliary atresia group was younger than the non-biliary atresia group.
Among the different laboratory investigations, platelets were significantly decreased among the biliary atresia group than in the non-biliary atresia group. While direct bilirubin, GGT, and aminotransferase platelet ratio index were significantly higher among the biliary atresia group than in the non-biliary atresia group. Previous studies have shown that the stiffness values could be affected by intrahepatic cholestasis, which was closely related to the level of bilirubin [7, 8].
Thirty patients had liver biopsies in our study. de Lédinghen et al. [10] investigated the utility of liver biopsies in cases of neonatal jaundice and stated that liver biopsy can correctly predict obstruction in more than 90% of cases, with a reported accuracy rate ranging between 60 and 95. In our study, there was a statistically significant relationship between the degree of fibrosis and APRI score; in the same context, de Lédinghen et al. [10] showed that the APRI significantly correlated to fibrosis grades in children with chronic liver diseases, including BA. Also, Sang Yong Kim et al. [11] determined the accuracy and reliability of the APRI in assessing fibrosis and histopathologic stage in patients with BA at the time of the Kasai portoenterostomy (HPE). In our study, there was a statistically significant relationship between the degree of fibrosis and SWE score (p = 0.002). These findings are suggestive that non-invasive determination of the stage of liver fibrosis in infants with cholestasis is a possibility and could help plan better clinical management. In the same line, Chen et al. [12] demonstrated that 2D SWE values correlated well with the pathological stages of liver fibrosis in a large sample of jaundiced infants with suspected BA. Additionally, 2D SWE demonstrated superiority over serum fibrosis markers, including the APRI score. Furthermore, 2D SWE has been widely used for evaluating liver fibrosis in adults with chronic liver diseases [13]. Several studies demonstrated that 2D SWE could accurately assess liver fibrosis in children with jaundice [8, 9, 14]. Our SWE values showed the most significant diagnostic performance in predicting the stage of liver fibrosis compared to APRI and other serum fibrosis markers; therefore, the preoperative measurement of liver stiffness may be helpful for diagnosis and treatment. ROC curve analysis in our study showed that the best cut-off value for SWE in measuring and discriminating patients with or without biliary atresia was 1.97 with a sensitivity of 75.0% and specificity of 83.5%, area under the curve of 0.819 (95% CI=0.699–0.937) for predicting the type of atresia (biliary/non-biliary), with positive and negative predictive values of 82.8% and 74.1%, respectively. Dong et al. [15] extracted the raw data for diagnostic test accuracy, and then these were used to examine the accuracy of ultrasound elastography for the diagnosis of BA. Among the 14 included studies, the cut-off value in BA cases is 1.92 m/s (range: 1.84–2.0 m/s) and 1.6 m/s (range: 1.53–1.77 m/s) in non-BA cases. Leschied et al. [16] examined eleven children younger than 1 year who had suspected liver disease and underwent hepatic shear wave elastography and clinically indicated percutaneous core needle biopsy. Using the VTQ mode, the mean liver shear wave speed was 2.08 ± 0.17 m/s for the biliary atresia group and 1.28 ± 0.13 m/s for the non-biliary atresia group (P < 0.0001).
Our post-Kasi patients were followed up 3 months post-operatively; their mean age was 2.5 months, with no significant influence on the procedure's outcome. Direct bilirubin was significantly decreased post-Kasai state compared to the pre-Kasai state. SWE measurements weren’t significantly accurate in differentiating between successful and failed Kasai operations, which is not the case in a study conducted by Yoon et al. [17], who followed up the patients on days 3, 5, and 7 post-operatively and whose poor outcome group included 5 patients with intractable cholangitis and three undergoing liver transplantation and showed high postoperative liver SWE values, which may be a reflection of early post-operative inflammation and elevated intracellular pressure.
Although these precursory data are encouraging, we faced certain limitations in this study. First, the number of patients in each group was not sufficient, so the future recommendation is to enlist more patients to further validate the results. Second, our Post Kasi follow-up of patients required a longer period for those surviving.
Conclusion
The results of this study suggest that shear-wave elastography is a useful diagnostic tool for differentiating biliary atresia from other causes of cholestasis in pediatric patients, with a high sensitivity and specificity. Further studies are needed to validate the findings and determine the optimal cut-off value for SWE in clinical practice.
Acknowledgments
Not applicable.
Author contributions
Aya bahaa and Wessam El-zayat done the ultrasound and shear-wave elastography, Noha Adel performed the liver biopsy and obtained the clinical data and Sally Emad was a major contributor to writing the manuscript. All authors read and approved the final manuscript.
Funding
No funding was obtained for this study.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.
Declarations
Ethics approval and consent to participate
All procedures were carried out in accordance with the ethical standards of the institutional committee. The study received the approval of the ethical committee of the Faculty of Medicine, Cairo University (Code: MD-329-2020).
Consent for publication
Written informed consent was obtained from the parents or caregivers for the publication of this study and accompanying images.
Competing interests
The authors declare that they have no competing interests.
List of Abbreviations
Alkaline phosphatase
Alanine transaminase
Aspartate transaminase-to-platelet ratio index
Acoustic radiation force impulse
Aspartate transaminase
Biliary atresia
Blood pressure
Complete blood count
Gamma-glutamyl transferase
Haemoglobin
Hepatoiminodiacetic acid
Hepatoportoenterostomy
Heart rate
International normalized ratio
Platelet
Prothrombin time
Respiratory rate
Shear wave elastography
Triangular cord
Ultrasonography
Virtual touch tissue imaging quantification
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
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Abstract
Background
The study aims to investigate Shear Wave Elastography's accuracy in assessing pediatric cholestasis and differentiating biliary atresia from other causes. The early diagnosis of cholestasis in newborns, when caused by true liver disease and not physiological or transient jaundice is usually eluded. To maximize the diagnostic reliability of ultrasound as an initial imaging modality to diagnose biliary atresia, ultrasound elastography has been introduced as a quantitative non-invasive sonographic technique to measure liver stiffness which is presumed to be different in biliary atresia from other cholestasis as well as follow-up liver stiffness post-Kasai operation.
Results
Ten patients (34.48%) were diagnosed with cholestasis with normal/low GGT. Five patients (17.24%) were diagnosed with hepatitis, and 2 patients had syndromes (10.34%). Other causes were found in 11 patients (37.93%). Major bile duct obstruction with fibrosis/cirrhosis was the majority of findings found in biliary atresia patients (100%), most of them with mild fibrosis (40%), followed by moderate (36.67%), then marked fibrosis (13.33%) and secondary cirrhosis (10%). ROC curve analysis shows that the best cut-off value for SWE = 1.97 with a sensitivity of 75.0% and specificity of 83.5%, with positive and negative predictive values were 82.8% and 74.1%, respectively. Mean shear wave elastography was significantly higher among the biliary atresia group (median 2.86) than in non-biliary atresia (median 1.81) and control groups (median 1.64) (P < 0.001) The best cut-off value of shear wear elastography for predicting outcome in pediatric patients post-Kasai procedure was 3.55, with a sensitivity of 66.7%, specificity of 64.7%, positive and negative predictive values were 25% and 91.7% respectively, with accuracy 65%.
Conclusion
The results of this study suggest that shear-wave elastography is a useful diagnostic tool for differentiating biliary atresia from other causes of cholestasis in pediatric patients, with a high sensitivity and specificity. Further studies are needed to validate the findings and determine the optimal cut-off value for shear wear elastography in clinical practice.
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Details
1 Cairo University Hospitals, Diagnostic and Intervention Radiology Department, Cairo, Egypt (GRID:grid.476980.4)
2 Cairo University Hospitals, Gasteroenterology Unit, Pediatric Department, Cairo, Egypt (GRID:grid.476980.4)