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World Journal of
Gastroenterology
ISSN 1007-9327 (print)
ISSN 2219-2840 (online)
World J Gastroenterol 2022 August 28; 28(32): 4475-4743
Published by Baishideng Publishing Group Inc
WJG https://www.wjgnet.com IAugust 28, 2022 Volume 28 Issue 32
World Journal of
Gastroenterology
W J G
Contents Weekly Volume 28 Number 32 August 28, 2022
REVIEW
Colon mucus in colorectal neoplasia and beyond
4475
Loktionov A
MINIREVIEWS
Who to screen and how to screen for celiac disease
4493
Singh P, Singh AD, Ahuja V, Makharia GK
Assessment of physical stress during the perioperative period of endoscopic submucosal dissection
4508
Chinda D, Shimoyama T
Expanding beyond endoscopy: A review of non-invasive modalities in Barrett’s esophagus screening and
surveillance
4516
Shahsavari D, Kudaravalli P, Yap JEL, Vega KJ
Impact of microbiota-immunity axis in pancreatic cancer management
4527
Bartolini I, Nannini G, Risaliti M, Matarazzo F, Moraldi L, Ringressi MN, Taddei A, Amedei A
Liver Imaging Reporting and Data System criteria for the diagnosis of hepatocellular carcinoma in clinical
practice: A pictorial minireview
4540
Liava C, Sinakos E, Papadopoulou E, Giannakopoulou L, Potsi S, Moumtzouoglou A, Chatziioannou A, Stergioulas L,
Kalogeropoulou L, Dedes I, Akriviadis E, Chourmouzi D
Liver regeneration as treatment target for severe alcoholic hepatitis
4557
Virovic-Jukic L, Ljubas D, Stojsavljevic-Shapeski S, Ljubičić N, Filipec Kanizaj T, Mikolasevic I, Grgurevic I
ORIGINAL ARTICLE
Basic Study
Wumei pills attenuates 5-fluorouracil-induced intestinal mucositis through Toll-like receptor 4/myeloid
differentiation factor 88/nuclear factor-κB pathway and microbiota regulation
4574
Lu DX, Liu F, Wu H, Liu HX, Chen BY, Yan J, Lu Y, Sun ZG
Sirolimus increases the anti-cancer effect of Huai Er by regulating hypoxia inducible factor-1α-mediated
glycolysis in hepatocellular carcinoma
4600
Zhou L, Zhao Y, Pan LC, Wang J, Shi XJ, Du GS, He Q
Anti-tumour activity and toxicological studies of combination treatment of Orthosiphon stamineus and
gemcitabine on pancreatic xenograft model
4620
Yehya AHS, Subramaniam AV, Asif M, Kaur G, Abdul Majid AMS, Oon CE
WJG https://www.wjgnet.com II August 28, 2022 Volume 28 Issue 32
World Journal of Gastroenterology
Contents Weekly Volume 28 Number 32 August 28, 2022
The mechanism of Yinchenhao decoction in treating obstructive-jaundice-induced liver injury based on
Nrf2 signaling pathway
4635
Liu JJ, Xu Y, Chen S, Hao CF, Liang J, Li ZL
Anoctamin 5 regulates the cell cycle and affects prognosis in gastric cancer
4649
Fukami T, Shiozaki A, Kosuga T, Kudou M, Shimizu H, Ohashi T, Arita T, Konishi H, Komatsu S, Kubota T, Fujiwara H,
Okamoto K, Kishimoto M, Morinaga Y, Konishi E, Otsuji E
Effects of Granule Dendrobii on chronic atrophic gastritis induced by N-methyl-N'-nitro-N-
nitrosoguanidine in rats
4668
Wu Y, Li Y, Jin XM, Dai GH, Chen X, Tong YL, Ren ZM, Chen Y, Xue XM, Wu RZ
Retrospective Study
Machine learning predicts portal vein thrombosis after splenectomy in patients with portal hypertension:
Comparative analysis of three practical models
4681
Li J, Wu QQ, Zhu RH, Lv X, Wang WQ, Wang JL, Liang BY, Huang ZY, Zhang EL
Observational Study
International patterns in incidence and mortality trends of pancreatic cancer in the last three decades: A
joinpoint regression analysis
4698
Ilic I, Ilic M
Prospective Study
Differential diagnosis of different types of solid focal liver lesions using two-dimensional shear wave
elastography
4716
Guo J, Jiang D, Qian Y, Yu J, Gu YJ, Zhou YQ, Zhang HP
META-ANALYSIS
Use of shear wave elastography for the diagnosis and follow-up of biliary atresia: A meta-analysis
4726
Wagner ES, Abdelgawad HAH, Landry M, Asfour B, Slidell MB, Azzam R
LETTER TO THE EDITOR
Is endoscopic mucosal ablation a valid option for treating colon polyps?
4741
Liu XY, Ren RR, Wu C, Wang LY, Zhu ML
WJG https://www.wjgnet.com III August 28, 2022 Volume 28 Issue 32
World Journal of Gastroenterology
Contents Weekly Volume 28 Number 32 August 28, 2022
ABOUT COVER
Editorial Board Member of World Journal of Gastroenterology, PhD, MD, Associate Professor in Infectious Diseases,
Department of Mental Health and Public Medicine, University of Campania “Luigi Vanvitelli”, Naples 80130, Italy.
caterina.sagnelli@unicampania.it
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The primary aim of World Journal of Gastroenterology (WJG, World J Gastroenterol) is to provide scholars and readers
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research articles and communicate their research findings online. WJG mainly publishes articles reporting research
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RESPONSIBLE EDITORS FOR THIS ISSUE
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Submit a Manuscript: https://www.f6publishing.com World J Gastroenterol 2022 August 28; 28(32): 4726-4740
DOI: 10.3748/wjg.v28.i32.4726 ISSN 1007-9327 (print) ISSN 2219-2840 (online)
META-ANALYSIS
Use of shear wave elastography for the diagnosis and follow-up of
biliary atresia: A meta-analysis
Ellen S Wagner, Hussien Ahmed H Abdelgawad, Meghan Landry, Belal Asfour, Mark B Slidell, Ruba Azzam
Specialty type: Gastroenterology
and hepatology
Provenance and peer review:
Unsolicited article; Externally peer
reviewed.
Peer-review model: Single blind
Peer-review report’s scientific
quality classification
Grade A (Excellent): A, A
Grade B (Very good): 0
Grade C (Good): C
Grade D (Fair): 0
Grade E (Poor): 0
P-Reviewer: El-Karaksy H, Egypt;
Pop TL, Romania; Redkar RG,
India
Received: May 1, 2022
Peer-review started: May 1, 2022
First decision: June 19, 2022
Revised: July 10, 2022
Accepted: July 31, 2022
Article in press: July 31, 2022
Published online: August 28, 2022
Ellen S Wagner, Ruba Azzam, Pediatric Gastroenterology, Hepatology, and Nutrition, The
University of Chicago Medicine, Comer Children’ s Hospital, Chicago, IL 60637, United States
Hussien Ahmed H Abdelgawad, Department of Medicine, Zagazig University, Zagazig 44511,
Egypt, Egypt
Meghan Landry, Department of Pediatrics, The University of Chicago Medicine, Comer
Children’ s Hospital, Chicago, IL 60637, United States
Belal Asfour, Graduate School of Professional Education-Biomedical Informatics, University of
Chicago, Chicago, IL 60637, United States
Mark B Slidell, Department of Surgery, The University of Chicago Medicine, Comer Children’ s
Hospital, Chicago, IL 60637, United States
Corresponding author: Ruba Azzam, MD, MPH, Associate Professor, Pediatric Gastroenter-
ology, Hepatology, and Nutrition, The University of Chicago Medicine, Comer Children’ s
Hospital, 5841 S Maryland Ave MC 4065, Chicago, IL 60637, United States.
razzam@peds.bsd.uchicago.edu
Abstract
BACKGROUND
Timely differentiation of biliary atresia (BA) from other infantile cholestatic
diseases can impact patient outcomes. Additionally, non-invasive staging of
fibrosis after Kasai hepatoportoenterostomy has not been widely standardized.
Shear wave elastography is an ultrasound modality that detects changes in tissue
stiffness. The authors propose that the utility of elastography in BA can be
elucidated through meta-analysis of existing studies.
AIM
To assess the utility of elastography in: (1) BA diagnosis, and (2) post-Kasai fibro-
sis surveillance.
METHODS
A literature search identified articles that evaluated elastography for BA diagnosis
and for post-Kasai follow-up. Twenty studies met criteria for meta-analysis:
Eleven for diagnosis and nine for follow-up post-Kasai. Estimated diagnostic odds
ratio (DOR), sensitivity, and specificity of elastography were calculated through a
random-effects model using Meta-DiSc software.
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4727 August 28, 2022 Volume 28 Issue 32
RESULTS
Mean liver stiffness in BA infants at diagnosis was significantly higher than in non-BA, with
overall DOR 24.61, sensitivity 83%, and specificity 79%. Post-Kasai, mean liver stiffness was
significantly higher in BA patients with varices than in patients without, with DOR 16.36,
sensitivity 85%, and specificity 76%. Elastography differentiated stage F4 fibrosis from F0-F3 with
DOR of 70.03, sensitivity 96%, and specificity 89%. Elastography also differentiated F3-F4 fibrosis
from F0-F2 with DOR of 24.68, sensitivity 85%, and specificity 81%.
CONCLUSION
Elastography has potential as a non-invasive modality for BA diagnosis and surveillance post-
Kasai. This paper’s limitations include inter-study method heterogeneity and small sample sizes.
Future, standardized, multi-center studies are recommended.
Key Words: Biliary atresia; Cholestasis; Hepatic portoenterostomy; Fibrosis; Esophageal and gastric varices;
Elasticity imaging techniques
©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
Core Tip: Ultrasound elastography is an emerging, non-invasive imaging modality to detect organ stiffness.
It may be a useful tool in biliary atresia (BA) diagnosis and post-Kasai fibrosis surveillance. In a meta-
analysis of twenty existing studies (eleven for diagnosis and nine for follow-up), this paper shows that
mean liver stiffness is significantly higher in BA patients compared to non-BA patients at time of
diagnosis. Post-Kasai, elastography can differentiate between early and advanced fibrosis as well as help
to discern the presence or absence of varices. While there are limitations to this analysis, elastography
shows great promise for its utility as a non-invasive modality for BA patients.
Citation: Wagner ES, Abdelgawad HAH, Landry M, Asfour B, Slidell MB, Azzam R. Use of shear wave
elastography for the diagnosis and follow-up of biliary atresia: A meta-analysis. World J Gastroenterol 2022;
28(32): 4726-4740
URL: https://www.wjgnet.com/1007-9327/full/v28/i32/4726.htm
DOI: https://dx.doi.org/10.3748/wjg.v28.i32.4726
INTRODUCTION
Biliary atresia (BA) is a progressive, fibroinflammatory disease of the biliary system that exclusively
affects infants. It accounts for about 30% of all cases of prolonged cholestasis in the first three months of
life[1]. Its incidence is estimated to be approximately 1:10000-19000 live births, with increased
prevalence in East Asian countries to up to 1:2700[2]. The initial clinical manifestations include
progressive jaundice, deep-colored urine, light colored stools, and an increase in conjugated serum
bilirubin levels. The similarity in clinical presentation and blood biochemistry results between patients
with BA and those with other infantile cholestatic liver diseases represents a great challenge to clinicians
in accurately establishing a final diagnosis in a timely fashion. Early identification of BA in an infant
with cholestatic jaundice is crucial, as the Kasai portoenterostomy (KPE) procedure may help restore
bile flow and prevent the otherwise rapid progression to biliary cirrhosis. A BA outcomes meta-analysis
by Jimenez-Rivera et al[2] included fourteen studies that focused on native liver survival (NLS), all of
which reported improved NLS when KPE was performed at an earlier age. Given its progressive nature,
BA is the most common indication for liver transplantation in the pediatric population, with NLS
ranging from 24.0% to 52.8% at ten years post-KPE[2]. Patients with BA who have undergone KPE need
close clinical monitoring to assess for signs of chronic liver disease progression, particularly as they
approach potential need for liver transplant. Currently, there are no widely accepted, validated non-
invasive tests to pre-operatively diagnose BA nor to evaluate for progressive fibrosis after KPE.
While ultrasound findings, such as absence of a contractile gall bladder after feeding or the presence
of a triangular cord sign, can be suggestive of BA, ultrasound alone is not diagnostic[3]. In order to
diagnose BA, a liver biopsy is performed to assess for the histopathologic signs of biliary obstruction,
portal edema, and fibrosis[4]. When performed at age 60 d or less, liver biopsy is 96.4% sensitive for the
diagnosis of BA[3]. The progressive nature of the disease makes it imperative that a diagnosis is made as
early as possible. The gold standard test to confirm BA is a formal cholangiogram. Assessment for
progression of chronic liver disease post-KPE is usually achieved by the constellation of findings on
laboratory and radiologic testing as well as consideration for repeat liver biopsy and/or upper
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4728 August 28, 2022 Volume 28 Issue 32
gastrointestinal endoscopy, with no standardized guidelines for non-invasive staging of hepatic fibrosis
nor timing for endoscopic evaluation for potential variceal evolution. Invasive procedures carry risks,
both procedural as well as those related to sedation or anesthesia[4]. Delays at each juncture, both in
diagnosis and in post-KPE surveillance, can have a potentially detrimental impact on patient outcome.
Ultrasound elastography (UE) is an emerging imaging modality that uses applied force via
ultrasound probe to measure the elastic properties of tissue[5,6]. UE can be classified into strain imaging
and shear wave imaging. Strain imaging relies on a normal external force (push) or intrinsic forces (i.e.,
respiration or cardiovascular movement) within the body. For this reason, strain imaging is difficult to
quantify and reproduce, particularly in deeper organs, leading to limited applicability in the liver. As a
result, strain imaging was not the focus of this analysis[7,8].
Shear wave imaging, also called shear wave elastography (SWE) utilizes a dynamic stress and can be
further classified into transient elastography (TE), point shear wave elastography (pSWE; also called
VTQ or Virtual Touch Quantification on some platforms), and two-dimensional shear wave
elastography (2D-SWE; also called VTIQ or Virtual Touch IQ on some platforms)[8,9]. TE, which is
performed using the FibroScan (Echosens, Paris, France) system, utilizes a mechanical punch to generate
forces and measure unidirectional pressure waves[5]. pSWE and 2D-SWE differ from TE in that they
utilize B mode ultrasound imaging guidance, which enables direct visualization of tissue, as well as an
acoustic radiation force impulse (ARFI) in order to measure tissue stress. pSWE enables the
measurement of average shear wave speed within a region of interest while 2D-SWE uses multiple foci
of tissue displacement along an axis to generate a quantitative map of shear wave speed[5].
SWE has been studied extensively in adult liver literature with studies in pediatric liver disease
emerging only recently[6]. And yet, while multiple authors have addressed the utility of SWE for
diagnosis and management in BA, there have been no large-scale studies nor meta-analyses on this
modality. The aim of this meta-analysis is to evaluate the utility of SWE in: (1) the differentiation of BA
from other cholestatic liver diseases of infancy, and (2) the assessment of fibrosis progression in post-
KPE follow-up.
MATERIALS AND METHODS
This review was conducted in strict accordance with the Cochrane handbook of systematic reviews of
interventions[10]. We followed the Preferred Reporting Items for Systematic Review and Meta-Analysis
of Diagnostic Test Accuracy studies (PRISMA-DTA statement)[11]. The review was publicly registered
with the Open Science Framework (OSF). The statistical analysis was performed by co-authors H.A.,
who has over four years as a biostatistician in a clinical research organization, and M.L., who is a clinical
research coordinator employed by the University of Chicago.
Search strategy and eligibility criteria
PubMed, Scopus, Web of Science, EBSCO, and Cochrane Central were searched for English language
studies with information on BA and elastography from 2010 to 2021. Two of the authors performed the
literature search using the keywords: “Elastography” AND “biliary atresia”.
Full texts were reviewed to select eligible studies for meta-analysis. Studies were included if the
following criteria were met: (1) The study used SWE to differentiate BA from other cholestatic liver
diseases of infancy; (2) the study used SWE in the follow-up of patients with BA for the development of
fibrosis/cirrhosis post-KPE; and (3) the study assessed the accuracy of SWE for the diagnosis or follow-
up of liver fibrosis based on the cut-off point for liver stiffness and/or spleen stiffness values.
Exclusion criteria were as follows: (1) Full text article was not available and/or abstract and article
were not available in English; (2) the study was not specific to BA and/or did not utilize SWE (3) the
study evaluated the accuracy of SWE combined with other diagnostic methods; (4) the study used SWE
as a reference test to study novel biomarkers; and (5) the study was a review article, letter to the editor,
case report, editorial, case series, or consensus statement. Only studies with reliable data for extraction
and analysis were included in the meta-analysis.
Data extraction
Two authors independently reviewed and extracted the data from each included study. Data were
extracted for study characteristics (e.g., first author and year of publication, study period, study setting,
study design, and sample size), baseline characteristics of the included patients (e.g., age of patients,
laboratory date, age at diagnosis), and diagnostic data (e.g., sensitivity, specificity, predictive values).
Risk of bias assessment
Two researchers assessed the risk of bias of studies included using version 2 of the Quality Assessment
of Diagnostic Test Accuracy Studies (QUADAS-2) tool[12]. QUADAS-2 examines seven items on the
representation of patient spectrum, selection criteria, reference standard, verification bias, timing, and
study withdrawals. Both reviewers scored the tool independently; all disagreements were discussed and
consensus was reached.
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4729 August 28, 2022 Volume 28 Issue 32
Data analysis
Heterogeneity was assessed by visual inspection of the forest plots and measured by I-square and Chi-
Square tests. In case of significant heterogeneity (P < 0.1), a random effect model was used. Continuous
data were pooled as standardized mean difference (SMD) in a meta-analysis model using inverse
variance method with the respective 95% confidence intervals. We used Comprehensive Meta Analysis
(CMA, United States) software version 3.3.070 for windows. Methods described in reference[13] were
utilized to compute missing standard deviations. The diagnostic accuracy indicators of each test were
pooled as sensitivity, specificity, and diagnostic odds ratio (DOR) with the corresponding 95%
confidence intervals by the DerSimonian-Laird random effect model using MetaDiSc Beta-1.4 software.
In addition, the Summary Receiver Operating Characteristic (SROC) curve was used for the evaluation
of diagnostic tests and represents the relationship between true positive and negative rates considering
the varying diagnostic thresholds among studies. The summary of the test performance was represented
with an AUC of 1.0 (100%) indicating perfect discriminatory ability to distinguish BA from non-BA.
Seven studies used SWE machinery that reported results in units of m/s as opposed to kPa, with four
being evaluated for diagnostic test accuracy[14-18] and two for utility of SWE for follow-up[19,20].
Values reported in m/s were converted to kPa as per reference[8] (Supplementary material).
RESULTS
Electronic search yielded 243 studies with 42 identified as potentially meeting inclusion criteria
(Figure 1). Full text articles were retrieved and assessed for final eligibility. After the review of all full
text articles, 22 were excluded due to study design and unreliable data for extraction, the use of SWE as
an adjunct to the primary study of a novel biomarker, and subject comparison to healthy controls (as
opposed to other cholestatic infants). Eleven studies on the utility of SWE in accurately differentiating
BA from other cholestatic liver diseases of infancy met criteria for inclusion, as well as nine studies that
evaluated the utility of SWE in assessing and monitoring the development of hepatic fibrosis/cirrhosis
post-KPE. The studies included were mostly single center, retrospective analyses conducted in infants
and children (age 0-18 years) and published in peer-reviewed journals between 2010 and 2021. Detailed
individual study characteristics are presented in Table 1.
The overall quality of the included studies assessed by the QUADAS-2 (Figure 2), was moderate to
high. All analyzed studies were found to have low risk of bias in five or more of the seven items, with
the exception of[21], which showed unclear risk of bias in two of seven items and high risk of bias in
patient selection. Unclear risk of bias was reported in patient selection due to lack of clear selection
criteria in several studies. Potential risk of bias in the index test was recorded in several studies due to
lack of reporting on blinding relative to reference standard results. Potential bias in reference standards
emerged due to the use of multiple different reference standards (surgical exploration, intraoperative
cholangiography, liver biopsy) with possibility for incorrect classification of BA. Finally, bias in the flow
and timing was primarily due to a lack of reported details in some of the included studies.
SWE for the diagnosis of BA
Data on SWE for distinguishing BA from other cholestatic neonatal liver diseases were collected from 11
studies with 1307 total patients (560 with BA and 747 without BA). The mean liver stiffness value was
significantly higher in the BA group compared to the non-BA group (overall SMD = 2.30 kPa, 95%CI:
1.69, 2.90, P < 0.0001). Pooled studies were heterogeneous (P < 0.01, I2 = 94%) (Figure 3). Of the 11
studies included, five reported on performing diagnostic test analysis using liver biopsy as the reference
test, one study[22] used surgical exploration or cholangiography, and the reference was not specified in
another[16].
The forest plot of sensitivity and specificity for the diagnostic performance of the liver stiffness value
measured by SWE for differentiating BA from other etiologies of neonatal cholestasis is shown in
Figure 4A. The pooled sensitivity was 83% (95%CI: 80%, 86%) and specificity was 79%, (95%CI: 76%,
82%). The SROC curves of SWE for the diagnosis of BA are illustrated in Figure 4B. The SROC curve
was symmetric, and the AUC was 0.91, Q was 0.84 (SE = 0.02). The DOR was 24.61, (95%CI: 12.74, 47.53,
I2 = 72.4%) as shown in Figure 4C. Two of the 11 articles did not report a cut-off value for differentiating
between BA and non-BA[14,15] and were excluded from this analysis.
SWE for the follow-up of patients with BA
Data on SWE to assess liver disease progression in post-KPE follow-up were collected from nine studies
including 327 total patients [101 patients with varices, 124 patients without varices, 41 patients with
fibrosis (F0-F2), and 61 patients with fibrosis (F3-F4)]. Fibrosis stage is reported via METAVIR standards,
a scale from F0 to F4 where F0 shows no signs of histologic fibrosis, F2 represents moderate fibrosis with
few bridges/septa, F3 is numerous septa without cirrhosis, and F4 signifies cirrhosis.
The mean liver stiffness value was significantly higher in patients with varices in comparison to
patients without varices (overall SMD 1.38 kPa, 95%CI: 1.02, 1.74, P < 0.00001). Pooled studies were
homogenous (P = 0.29, I2 = 19%) (Figure 5A). Only three studies reported data on the diagnostic
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4730 August 28, 2022 Volume 28 Issue 32
Table 1 Main characteristics of studies included in the meta-analysis
Ref. Country Study design
Elastography
Method; machine;
probe, if specified
Reference
standard
Sample
size
Type of
patient Main finding
Diagnosis
Hanquinet et al
[14], Pediatric
Radiology, 2015
Switzerland Single center
retrospective
analysis
pSWE (VTQ);
Acuson S2000 or
S3000 (Siemens
Healthcare,
Erlangen, Germany)
Liver biopsy;
Cholangiogram
20 Cholestatic
infants;
mean age
52.1 d
Utilizing SWE in addition to
standard abdominal ultrasound
can provide useful information
on liver fibrosis to aid in the
diagnosis of BA
Leschied et al
[15], Pediatric
Radiology, 2015
USA Prospective
cohort
pSWE (VTQ) and
2D-SWE (VTIQ),
Acuson S3000
(Siemens
Healthcare,
Erlangen, Germany);
9L4 Transducer
Liver biopsy;
Cholangiogram
11 Infants with
suspected
liver
disease;
mean age
3.8 mo
Shear wave speeds were
significantly higher in children
with BA than those without
Wang et al[31],
Journal of
Ultrasound
Medicine, 2016
China Single center
case control
pSWE; Aixplorer
(SuperSonic Imagine
SA, Aix-en-
Provence, France);
L15-4 linear probe
KPE 38 Cholestatic
infants age
16 to 140 d
Mean shear wave speeds were
higher for BA patients than non-
BA cholestatic patients and
control patients
Zhou et al [22],
European
Radiology, 2017
China Single center
prospective
analysis
pSWE; Aixplorer
(SuperSonic Imagine
SA, Aix-en-
Provence, France);
SL15-4 linear array
transducer
Liver biopsy;
Cholangiogram;
surgical
exploration
172 Cholestatic
infants, age
2 to 140 d
SWE is useful to differentiate
BA from non-BA; its
performance does not
outperform grey scale
ultrasound
Wu et al[32],
Hepatology, 2018
Taiwan Single center
prospective
analysis
TE; FibroScan 502
Touch (Echosens,
Paris, France); S1
probe
Liver biopsy;
cholangiogram
48 Cholestatic
infants, age
35 to 61 d
Liver stiffness assessment
during the work up of
cholestatic infants may facilitate
diagnosis of BA
Dillman et al[16],
Journal of
Pediatrics, 2019
USA Multiple center
prospective
analysis
2D-SWE (VTIQ) and
pSWE (VTQ);
Acuson S2000 or
S3000 (Siemens
Healthcare,
Erlangen, Germany);
9L4 linear
transducer probe
Not specified 41 Cholestatic
infants, age
24 to 52 d
SWE and GGT can help
discriminate BA from other
causes of cholestasis
Duan et al[33],
BioMed Research
International, 2019
China Single center
case control
2D-SWE; TUS-Aplio
500 (Canon Medical
Systems, Tokyo,
Japan); 14L5 linear
array probe
Liver biopsy;
KPE
138 Cholestatic
infants, age
5-90 d
SWE can help distinguish BA
from other cholestatic diseases;
the diagnostic specificity
increases when combined with
grey-scale ultrasound
Chen et al[17],
European
Radiology, 2020
China Single center
multiple
method
(prospective
and
retrospective)
analysis
pSWE (VTQ);
Acuson S2000
(Siemens
Healthcare,
Erlangen, Germany);
4-9MHz linear
transducer
Liver biopsy;
cholangiogram
308 in
subgroup
1; 187 in
subgroup
2
Cholestatic
infants, age
under 100 d
Shear wave speed, coupled with
presence of triangular cord sign,
provided moderate-to-high
accuracy for BA diagnosis. This
study also found high
diagnostic performance in a risk
stratification model built on five
predictors (shear wave speed,
triangular cord sign, GGT,
abnormal gallbladder, clay-
colored stool)
Liu et al[18],
International
Journal of Clinical
Practice, 2020
China Single center
retrospective
analysis
2D-SWE (VTIQ) and
pSWE (VTQ);
Acuson OXANA2
(Siemens
Healthcare,
Erlangen, Germany);
3-5.5 MHz-6C1
convex and 4-9MHz
9L4 linear array
probe
Surgical
exploration
59 Cholestatic
infants, age
25 to 141 d
VTQ and VTIQ can help
distinguish BA from non-BA in
cholestatic infants; VTIQ has
higher sensitivity and specificity
than VTQ
pSWE; Aixplorer
(SuperSonic Imagine
SA, Aix-en-
Liver stiffness measurements
and GGT values have the
potential to decrease rates of BA
Shen et al[34],
BMC Pediatrics,
2020
China Single center
retrospective
analysis
Not specified 282 Cholestatic
infants, age
under 120 d
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4731 August 28, 2022 Volume 28 Issue 32
Provence, France);
L15-4 linear probe
misdiagnosis
Wang et al[35],
Academic
Radiology, 2020
China Single center
prospective
analysis
2D-SWE; Aixplorer
(SuperSonic Imagine
SA, Aix-en-
Provence, France);
linear probe
Liver biopsy;
Cholangiogram
294 Cholestatic
infants, age
under 70 d
Age, gallbladder morphology,
and liver elasticity incorporated
together into a nomogram
shows an improved predictive
value for BA diagnosis
Follow-up
Chongsrisawat et
al[36], BMC
Gastroenterology,
2011
Thailand Single center
prospective
analysis
TE; FibroScan 502
Touch (Echosens,
Paris, France)
Endoscopy 73 BA patients
after KPE,
mean age
9.11 yr
TE is useful for predicting the
presence of EV/GV in BA
patients post-KPE
Colecchia et al
[37], Digestive and
Liver Disease, 2011
Italy Single center
prospective
analysis
TE; FibroScan
(Echosens, Paris,
France)
Endoscopy 31 BA patients
after KPE,
age 4 to 25
yr
Non-invasive studies, such as
liver stiffness measurement, can
predict the presence of EV in BA
patients post-KPE
Shin et al[38],
Journal of
Ultrasound
Medicine, 2014
South
Korea
Single center
retrospective
analysis
TE; FibroScan 502
Touch (Echosens,
Paris, France); S or
M probe
Liver biopsy 47 BA patients,
mean age 60
d
TE may be a useful, non-
invasive method for diagnosing
severe fibrosis and cirrhosis;
may predict outcomes before
surgery or liver biopsy in
infants with BA
Shen et al[39],
World Journal of
Gastroenterology,
2015
China Single center
retrospective
analysis
TE; FibroScan
(Echosens, Paris,
France); S probe
Liver biopsy 31 BA patients,
age 34 to 121
d
TE can be a useful, non-invasive
technique to assess liver fibrosis
in children with BA. The cut-off
value of 15.15 kPa can
distinguish cirrhotic from non-
cirrhotic patients
Chen et al[40],
Nature Scientific
Reports, 2016
China Single center
retrospective
analysis
2D-SWE; Aixplorer
(SuperSonic Imagine
SA, Aix-en-
Provence, France);
SC-1 curvilinear
probe
Liver biopsy 24 BA patients
after KPE,
mean age
6.6 yr
2D-SWE has more promise as a
means of assessing liver fibrosis
in BA patients than APRI or
FIB-4 scoring
Tomita et al[20],
Pediatric Radiology
, 2016
Japan Single center
prospective
analysis
pSWE (VTQ);
Acuson S2000
(Siemens
Healthcare,
Erlangen, Germany);
4C1 probe
Liver biopsy;
endoscopy
28 BA patients,
age 0.1 to
33.6 yr
Liver and spleen stiffness
measured via ARFI has potential
as a non-invasive marker of
liver fibrosis and esophageal
varices in BA patients
Sintusek et al[41],
Journal of Pediatric
Gastroenterology
and Nutrition,
2019
Thailand Single center
prospective
analysis
TE; FibroScan
Compact 530
(Echosens, Paris,
France); S or M
probe
Endoscopy 51 BA patients
after KPE,
mean age
10.63 yr
Spleen stiffness can predict the
presence of esophageal varices
in children with BA;
combination of spleen and liver
stiffness measurements to
diagnose varices increases
diagnostic yield
Yokoyama et al
[19], Hepatology
Research, 2019
Japan Single center
prospective
study
2D-SWE; Aplio i900
(Canon Medical
Systems, Tokyo,
Japan); i8CX1
transducer
Endoscopy 34 BA patients
after KPE,
age 1034 to
3940 d
Spleen stiffness (measured via
2D-SWE) is the most accurate
predictor of high risk
esophageal/gastric varices in
BA patients
Srisuwan et al
[21], Siriraj
Medical Journal,
2021
Thailand Single center
cross-sectional
study
TE; FibroScan 502
Touch (Echosens,
Paris, France); S or
M probe
Endoscopy 20 BA patients
after KPE,
age 2.3 to
21.0 yr
There is correlation between
liver stiffness measurement and
clinical/radiological evidence of
portal hypertension. TE can
predict presence of esophageal
varices with high sensitivity
Point SW: Point shear wave elastography; 2D SW: Two-dimensional shear wave elastography; VTIQ: Virtual Touch IQ, alternative nomenclature for two-
dimensional shear wave elastography; VTQ: Virtual touch quantification, alternative nomenclature for point Shear Wave Elastography; TE: Transient
elastography; KPE: Kasai hepatoportoenterostomy; BA: Biliary atresia; EV: Esophageal varices; GV: Gastric varices; ARFI: Acoustic radiation force impulse.
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4732 August 28, 2022 Volume 28 Issue 32
Figure 1 Preferred Reporting Items for Systematic Review and Meta-Analysis flow diagram of the meta-analysis.
performance of spleen stiffness measured by SWE for predicting the presence of varices in patients with
BA post-KPE. The mean spleen stiffness value was significantly higher in patients with varices when
compared to patients without varices (overall SMD 1.66 kPa, 95%CI: 1.19, 2.14, P < 0.00001). Pooled
studies were homogenous (P = 0.42, I2 = 0%) (Figure 5B).
The forest plot of the sensitivity and specificity for the diagnostic performance of liver stiffness value
measured by SWE to predict the presence of varices is shown in Figure 6A. The pooled sensitivity was
85% (95%CI: 77%, 91%), while the specificity was 76%, 95%CI (67%, 83%). Illustrated in Figure 6B, the
SROC curve was symmetric and the AUC was 0.86 with Q value of 0.80 (SE = 0.05). The DOR was 16.36,
95%CI (8.18, 32.70), I2 = 0%, showing no heterogeneity among the pooled studies (Figure 6C).
Three studies utilized spleen stiffness measured by SWE to predict the presence of varices with
endoscopy as a reference test. The pooled sensitivity was 84% (95%CI: 69%, 94%), while the specificity
was 84%, 95%CI (73%, 92%). The AUC of the SROC curve was 0.91, with Q value of 0.85 (SE = 0.403).
The DOR was 28.93, 95%CI (8.99, 93.14), I2 = 0%, showing no heterogeneity among the pooled studies
(Supplementary Figure 1).
Four studies used liver stiffness value measured by SWE to predict the presence of liver fibrosis F4
(vs F0-3) when liver biopsy was the reference test. The forest plot for the sensitivity and specificity of the
diagnostic performance of liver stiffness value measured by SWE to predict the presence of liver fibrosis
F4 is shown in Figure 7A. The pooled sensitivity was 96% (95%CI: 79%, 100%), while the specificity was
89%, (95%CI: 81%, 94%). The SROC curves of liver stiffness value measured by SWE are illustrated in
Figure 7B. The AUC of the SROC curve was 0.95, with Q value of 0.89 (SE = 0.04). The DOR was 70.04,
(95%CI: 16.06, 305.40), I2 = 0%, showing no heterogeneity among the pooled studies (Figure 7C).
Three studies used the liver stiffness value measured by SWE to predict the presence of liver fibrosis
F3-4 (vs F0-2) when liver biopsy was the reference test. The pooled sensitivity was 85% (95%CI: 71%,
94%), and specificity 81%, 95%CI (67%, 91%). The AUC of the SROC curve was 0.91, with Q value of 0.84
(SE = 0.04). The DOR was 24.68, 95%CI (7.43, 82.01), I2 = 0%, showing no heterogeneity among the
pooled studies (Supplementary Figure 2).
DISCUSSION
Early diagnosis of BA is crucial to patient outcomes. At present, diagnosis depends on invasive liver
biopsy and intraoperative cholangiogram. The present meta-analysis is the first to our knowledge to
assess the potential utility of preoperative SWE in establishing the diagnosis of BA. In our meta-
analysis, we observed that liver stiffness value measured by SWE had high diagnostic accuracy for
differentiating BA from other neonatal cholestasis (AUC = 0.91) with high summary sensitivity of 83%
as well as summary specificity of 79% and DOR of 24.61. Notably, several of the studies used different
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4733 August 28, 2022 Volume 28 Issue 32
Figure 2 Quality assessment by Quality Assessment of Diagnostic Test Accuracy Studies (QUADAS-2) of the included studies.
Figure 3 Forest plot comparing the liver stiffness value (Kpa) between the patients with and without biliary atresia. Dillman, Wang (2020),
Leschied, and Liu each have multiple analyses due to different shear wave elastography modes and/or phases of study (training, validation). Point SW: Point shear
wave elastography; 2D SW: Two-dimensional shear wave elastography; VTIQ: Virtual touch IQ, alternative nomenclature for two-dimensional shear wave
elastography; VTQ: Virtual touch quantification, alternative nomenclature for point shear wave elastography.
Wagner E et al. SWE for BA
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Figure 4 Forest plot of liver stiffness value measured by shear wave elastography to differentiate biliary atresia from other neonatal
cholestasis. A: Diagnostic sensitivity and specificity; B: Summary receiver operating characteristic curve; C: Diagnostic odds ratio. Point SW: Point shear wave
elastography; 2D SW: Two-dimensional shear wave elastography; VTIQ: Virtual touch IQ, alternative nomenclature for two-dimensional shear wave elastography;
VTQ: Virtual touch quantification, alternative nomenclature for point shear wave elastography.
reference standards (five utilized liver biopsy, one utilized surgical exploration or cholangiography, and
one did not specify its reference standard). When interpreted within the context of pathophysiology of
BA, with fibrosis beginning at bile duct obliteration, in comparison to non-BA cholestasis which has
variable degrees of fibrosis, these results reflect the potential for SWE to aid in the diagnostic process.
Post-KPE, a significant number of patients develop persistent cholestasis, portal hypertension, and
progressive fibrosis. Risk stratification for these patients continues to be a clinical challenge for hepato-
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Figure 5 Forest plot comparing liver and spleen stiffness value between post-Kasai patients with or without varices. A: The liver stiffness
value (Kpa); B: Spleen stiffness value (Kpa).
logists. The second portion of this analysis explored the potential utility of SWE for accurately assessing
the progression of hepatic fibrosis post-KPE. We observed significant differences in liver and spleen
stiffness in patients with varices. The diagnostic accuracy of liver stiffness value measured by SWE was
similar to spleen stiffness value to predict the presence of varices post-KPE (AUC = 0.86 and 0.92,
respectively). The pooled sensitivity was comparable between liver stiffness and spleen stiffness (85% vs
84%), but the pooled specificity of spleen stiffness was higher than liver stiffness (84% vs 76%). Notably,
only three studies investigated spleen stiffness and five investigated liver stiffness to predict the
presence of post-KPE varices.
This analysis also demonstrated significant predictive efficacy for the presence and severity of biopsy-
proven liver fibrosis in four studies. Liver stiffness value measured by SWE to determine advanced liver
fibrosis (F4 vs F0-3) has high diagnostic accuracy (AUC = 0.95), sensitivity (96%) and specificity (89%).
Liver stiffness value measured by SWE to differentiate between F3-4 and F0-2 fibrosis has a lower
diagnostic accuracy (AUC = 0.91), with sensitivity (85%) and specificity (81%). This is in line with
studies in the adult literature, which have found increased accuracy of SWE for high grade (stage F3-4)
fibrosis in comparison to F0-F2[23].
Although the findings from this meta-analysis are compelling, there are notable limitations to the
analysis. The studies included in this analysis were mostly small and single-center, which limits general-
izability across large, non-homogenous populations. Furthermore, each study analyzed for BA
diagnosis was performed on infants of different average age (with ranges from two to 140 d of life);
given the rapid evolution of fibrosis in BA, the variety of ages analyzed may influence the results.
In addition to the use of different reference standards (liver biopsy vs surgical exploration or cholan-
giogram), there were notable differences in methodology from study to study, in particular regarding
patients’ fasting status and sedation, sonographer characteristics (blinded vs non-blinded, level of
expertise, etc.), number of measurements obtained, and measurement quality standards. Previous
analyses of SWE technology have highlighted significant differences in results obtained depending on
sedation and fasting status, operator dependence, and probe choice[5,24-27]. This demonstrates the
importance of methodological unity in comparison between data sets. While our results are promising,
this is an important implication in terms of broad applicability of our meta-analysis and the need for
further, well-designed trials to address the potential utility of SWE in BA.
Patient factors aside, several study centers utilized different SWE platforms (TE vs pSWE vs 2D-SWE)
and machines (detailed in Table 1), each of which reported results in either kPa or m/s. As such,
analysis relied upon interconversion of results from Young’s modulus to shear modulus (kPa to m/s)
[7]. While there is a well-documented mathematical proof enabling this interconversion, the proof relies
upon assumptions about tissue characteristics, notably that the tissue has constant density and
homogeneity, displays isotropic and elastic characteristics, and is linear under compressible stress (
Supplementary material)[7,8]. The inherent characteristics of an inflamed, potentially fibrotic liver do
not fit well into this description, which is important to mention given an analysis that relies heavily on
Wagner E et al. SWE for BA
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Figure 6 Forest plot of liver stiffness value measured by shear wave elastography to predict the presence of varices in post-Kasai
patients. A: Diagnostic sensitivity and specificity; B: Summary receiver operating characteristic curve; C: Diagnostic odds ratio.
interconversion between results[28,29]. In a similar vein, a recent study by Darweesh et al[30] found that
cholestasis itself can increase liver stiffness measurements in adult patients, separate to histologic
findings of fibrosis; future studies must take this potential confounder into account. This meta-analysis
must be interpreted within the context of these limitations, with future studies taking important steps to
address potential limitations and barriers to interpretation during the study design, data collection and
analysis phases of work.
CONCLUSION
Despite non-standardized methodology across analyzed articles as well as reliance upon data intercon-
version, this meta-analysis highlights the potential of SWE as a non-invasive method to assist in both the
diagnosis as well as post-KPE follow-up of BA. Further standardized, multi-center studies are needed in
order to better elucidate this potential. By applying uniform methods, machinery, and data reporting (in
Wagner E et al. SWE for BA
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Figure 7 Forest plot of liver stiffness value measured by shear wave elastography to predict the presence of liver fibrosis F4 (vs F0-3) in
post-Kasai patients. A: Diagnostic sensitivity and specificity; B: Summary receiver operating characteristic curve; C: Diagnostic odds ratio.
either kPa or m/s), further studies may be able to identify SWE as a non-invasive tool with utility both
in diagnosis of BA as well as post-KPE prediction of outcomes.
ARTICLE HIGHLIGHTS
Research background
Biliary atresia (BA) is a progressive infantile cholestatic disease. Diagnosis is confirmed by intra-
operative cholangiogram; any delays to diagnosis and palliating Kasai hepatoportoenterostomy can
increase the odds of needing liver transplant. Following Kasai, patients will need surveillance for
progression of liver disease, which often requires liver biopsy.
Wagner E et al. SWE for BA
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Research motivation
Because the diagnosis and surveillance of BA both involve invasive procedures, there are risks for delay
and/or adverse outcomes at each stage. By using non-invasive shear wave elastography (SWE), which
measures changes in tissue stiffness, to identify liver stiffness thresholds for BA diagnosis and evolution
of fibrosis post-Kasai, clinicians may be able to accurately diagnose and surveil BA without invasive
procedures.
Research objectives
The authors performed a meta-analysis on studies into the utility of SWE for BA diagnosis and post-
Kasai surveillance in order to determine whether existing literature could help identify liver stiffness
thresholds for BA diagnosis and development of fibrosis post-Kasai.
Research methods
A literature search yielded twenty studies, eleven for diagnosis and nine for follow-up post-Kasai.
Diagnostic odds ratio (DOR), sensitivity, and specificity of elastography were calculated through a
random-effects model.
Research results
Mean liver stiffness in BA infants was higher than in cholestatic infants without BA with DOR 24.61,
sensitivity 83%, specificity 79%. Mean liver stiffness post-Kasai was significantly higher in patients with
varices than those without (DOR 16.36, sensitivity 85%, specificity 76%). SWE differentiated METAVIR
F4 fibrosis from F0-F3 (DOR 70.03, sensitivity 96%, specificity 89%) as well as F3-F4 fibrosis from F0-F2
(DOR 24.68, sensitivity 85%, specificity 81%).
Research conclusions
SWE may be a useful, non-invasive modality for the diagnosis and post-Kasai surveillance in BA. The
analysis is limited by methodological heterogeneity between studies as well as small sample sizes.
Research perspectives
In order for SWE to be useful for future BA cases, larger, standardized, multi-center studies are
recommended to establish appropriate protocols.
FOOTNOTES
Author contributions: Wagner ES performed literature search, data acquisition and interpretation, manuscript
drafting, and final approval; Abdelgawad HAH performed data acquisition, statistical analysis and interpretation,
manuscript structure, drafting, and revisions; Landry M performed statistical analysis and interpretation, manuscript
structure and revisions; Asfour B performed figure compilation and manuscript revisions; Slidell MB performed
manuscript compilation, revisions, and final approval; Azzam R performed project structure, data acquisition and
interpretation, manuscript revisions, and final approval.
Conflict-of-interest statement: There are no conflicts of interest to report.
PRISMA 2009 Checklist statement: The authors have read the PRISMA 2009 Checklist, and the manuscript was
prepared and revised according to the PRISMA 2009 Checklist.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by
external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-
NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license
their derivative works on different terms, provided the original work is properly cited and the use is non-
commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Country/Territory of origin: United States
ORCID number: Ellen S Wagner 0000-0003-2013-5255; Hussien Ahmed H Abdelgawad 0000-0001-7101-837X; Meghan
Landry 0000-0001-9822-5117; Belal Asfour 0000-0002-6562-6229; Mark B Slidell 0000-0002-9551-5888; Ruba Azzam 0000-
0003-0151-2123.
S-Editor: Chen YL
L-Editor: A
P-Editor: Cai YX
Wagner E et al. SWE for BA
WJG https://www.wjgnet.com 4739 August 28, 2022 Volume 28 Issue 32
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