Predicting gastroesophageal varices through spleen magnetic resonance elastography in pediatric liver fibrosis
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摘要
BACKGROUND A recent retrospective study confirmed that hepatic stiffness and splenic stiffness measured with magnetic resonance elastography(MRE) are strongly associated with the presence of esophageal varices. In addition, strong correlations have been reported between splenic stiffness values measured with MRE and hepatic venous pressure gradients in animal models. However, most studies have been conducted on adult populations, and previous pediatric MRE studies have only demonstrated the feasibility of MRE in pediatric populations, while the actual clinical application of spleen MRE has been limited.AIM To assess the utility of splenic stiffness measurements by MRE to predict gastroesophageal varices in children.METHODS We retrospectively reviewed abdominal MRE images taken on a 3 T system in pediatric patients. Patients who had undergone Kasai operations for biliary atresia were selected for the Kasai group, and patients with normal livers and spleens were selected for the control group. Two-dimensional spin-echo echoplanar MRE acquisition centered on the liver, with a pneumatic driver at 60 Hz and a low amplitude, was performed to obtain hepatic and splenic stiffness values. Laboratory results for aspartate aminotransferase to platelet ratio index(APRI) were evaluated within six months of MRE, and the normalized spleen size ratio was determined with the upper normal size limit. All Kasai group patients underwent gastroesophageal endoscopy during routine follow-up. The MannWhitney U test, Kendall's tau b correlation and diagnostic performance analysis using the area under the curve(AUC) were performed for statistical analysis.RESULTS The median spleen MRE value was 5.5 kPa in the control group(n = 9, age 9-18 years, range 4.7-6.4 kPa) and 8.6 kPa in the Kasai group(n = 22, age 4-18 years,range 5.0-17.8 kPa). In the Kasai group, the APRI, spleen size ratio and spleen MRE values were higher in patients with portal hypertension(n = 11) than in patients without(n = 11)(all P < 0.001) and in patients with gastroesophageal varices(n = 6) than in patients without(n = 16)(all P < 0.05), even though their liver MRE values were not different. The APRI(τ = 0.477, P = 0.007), spleen size ratio(τ = 0.401, P = 0.024) and spleen MRE values(τ = 0.426, P = 0.016) also correlated with varices grades. The AUC in predicting gastroesophageal varices was 0.844 at a cut-off of 0.65(100% sensitivity and 75% specificity) for the APRI,and 0.844 at a cut-off of 9.9 kPa(83.3% sensitivity and 81.3% specificity) for spleen MRE values.CONCLUSION At a cut-off of 9.9 kPa, spleen MRE values predicted gastroesophageal varices as well as the APRI and spleen size ratio in biliary atresia patients after the Kasai operation. However, liver MRE values were not useful for this purpose.
BACKGROUND A recent retrospective study confirmed that hepatic stiffness and splenic stiffness measured with magnetic resonance elastography(MRE) are strongly associated with the presence of esophageal varices. In addition, strong correlations have been reported between splenic stiffness values measured with MRE and hepatic venous pressure gradients in animal models. However, most studies have been conducted on adult populations, and previous pediatric MRE studies have only demonstrated the feasibility of MRE in pediatric populations, while the actual clinical application of spleen MRE has been limited.AIM To assess the utility of splenic stiffness measurements by MRE to predict gastroesophageal varices in children.METHODS We retrospectively reviewed abdominal MRE images taken on a 3 T system in pediatric patients. Patients who had undergone Kasai operations for biliary atresia were selected for the Kasai group, and patients with normal livers and spleens were selected for the control group. Two-dimensional spin-echo echoplanar MRE acquisition centered on the liver, with a pneumatic driver at 60 Hz and a low amplitude, was performed to obtain hepatic and splenic stiffness values. Laboratory results for aspartate aminotransferase to platelet ratio index(APRI) were evaluated within six months of MRE, and the normalized spleen size ratio was determined with the upper normal size limit. All Kasai group patients underwent gastroesophageal endoscopy during routine follow-up. The MannWhitney U test, Kendall's tau b correlation and diagnostic performance analysis using the area under the curve(AUC) were performed for statistical analysis.RESULTS The median spleen MRE value was 5.5 kPa in the control group(n = 9, age 9-18 years, range 4.7-6.4 kPa) and 8.6 kPa in the Kasai group(n = 22, age 4-18 years,range 5.0-17.8 kPa). In the Kasai group, the APRI, spleen size ratio and spleen MRE values were higher in patients with portal hypertension(n = 11) than in patients without(n = 11)(all P < 0.001) and in patients with gastroesophageal varices(n = 6) than in patients without(n = 16)(all P < 0.05), even though their liver MRE values were not different. The APRI(τ = 0.477, P = 0.007), spleen size ratio(τ = 0.401, P = 0.024) and spleen MRE values(τ = 0.426, P = 0.016) also correlated with varices grades. The AUC in predicting gastroesophageal varices was 0.844 at a cut-off of 0.65(100% sensitivity and 75% specificity) for the APRI,and 0.844 at a cut-off of 9.9 kPa(83.3% sensitivity and 81.3% specificity) for spleen MRE values.CONCLUSION At a cut-off of 9.9 kPa, spleen MRE values predicted gastroesophageal varices as well as the APRI and spleen size ratio in biliary atresia patients after the Kasai operation. However, liver MRE values were not useful for this purpose.
BACKGROUND A recent retrospective study confirmed that hepatic stiffness and splenic stiffness measured with magnetic resonance elastography(MRE) are strongly associated with the presence of esophageal varices. In addition, strong correlations have been reported between splenic stiffness values measured with MRE and hepatic venous pressure gradients in animal models. However, most studies have been conducted on adult populations, and previous pediatric MRE studies have only demonstrated the feasibility of MRE in pediatric populations, while the actual clinical application of spleen MRE has been limited.AIM To assess the utility of splenic stiffness measurements by MRE to predict gastroesophageal varices in children.METHODS We retrospectively reviewed abdominal MRE images taken on a 3 T system in pediatric patients. Patients who had undergone Kasai operations for biliary atresia were selected for the Kasai group, and patients with normal livers and spleens were selected for the control group. Two-dimensional spin-echo echoplanar MRE acquisition centered on the liver, with a pneumatic driver at 60 Hz and a low amplitude, was performed to obtain hepatic and splenic stiffness values. Laboratory results for aspartate aminotransferase to platelet ratio index(APRI) were evaluated within six months of MRE, and the normalized spleen size ratio was determined with the upper normal size limit. All Kasai group patients underwent gastroesophageal endoscopy during routine follow-up. The MannWhitney U test, Kendall's tau b correlation and diagnostic performance analysis using the area under the curve(AUC) were performed for statistical analysis.RESULTS The median spleen MRE value was 5.5 kPa in the control group(n = 9, age 9-18 years, range 4.7-6.4 kPa) and 8.6 kPa in the Kasai group(n = 22, age 4-18 years,range 5.0-17.8 kPa). In the Kasai group, the APRI, spleen size ratio and spleen MRE values were higher in patients with portal hypertension(n = 11) than in patients without(n = 11)(all P < 0.001) and in patients with gastroesophageal varices(n = 6) than in patients without(n = 16)(all P < 0.05), even though their liver MRE values were not different. The APRI(τ = 0.477, P = 0.007), spleen size ratio(τ = 0.401, P = 0.024) and spleen MRE values(τ = 0.426, P = 0.016) also correlated with varices grades. The AUC in predicting gastroesophageal varices was 0.844 at a cut-off of 0.65(100% sensitivity and 75% specificity) for the APRI,and 0.844 at a cut-off of 9.9 kPa(83.3% sensitivity and 81.3% specificity) for spleen MRE values.CONCLUSION At a cut-off of 9.9 kPa, spleen MRE values predicted gastroesophageal varices as well as the APRI and spleen size ratio in biliary atresia patients after the Kasai operation. However, liver MRE values were not useful for this purpose.
引文
1 Serinet MO,Wildhaber BE,BrouéP,Lachaux A,Sarles J,Jacquemin E,Gauthier F,Chardot C.Impact of age at Kasai operation on its results in late childhood and adolescence:a rational basis for biliary atresia screening.Pediatrics 2009;123:1280-1286[PMID:19403492 DOI:10.1542/peds.2008-1949]
2 Chardot C,Buet C,Serinet MO,Golmard JL,Lachaux A,Roquelaure B,Gottrand F,BrouéP,Dabadie A,Gauthier F,Jacquemin E.Improving outcomes of biliary atresia:French national series 1986-2009.J Hepatol 2013;58:1209-1217[PMID:23402746 DOI:10.1016/j.jhep.2013.01.040]
3 Hartley JL,Davenport M,Kelly DA.Biliary atresia.Lancet 2009;374:1704-1713[PMID:19914515DOI:10.1016/S0140-6736(09)60946-6]
4 Hadzi?N,Davenport M,Tizzard S,Singer J,Howard ER,Mieli-Vergani G.Long-term survival following Kasai portoenterostomy:is chronic liver disease inevitable?J Pediatr Gastroenterol Nutr2003;37:430-433[PMID:14508212]
5 Piccinino F,Sagnelli E,Pasquale G,Giusti G.Complications following percutaneous liver biopsy.A multicentre retrospective study on 68,276 biopsies.J Hepatol 1986;2:165-173[PMID:3958472]
6 Pariente D,Franchi-Abella S.Paediatric chronic liver diseases:how to investigate and follow up?Role of imaging in the diagnosis of fibrosis.Pediatr Radiol 2010;40:906-919[PMID:20432008 DOI:10.1007/s00247-010-1600-3]
7 Bedossa P,Dargère D,Paradis V.Sampling variability of liver fibrosis in chronic hepatitis C.Hepatology 2003;38:1449-1457[PMID:14647056 DOI:10.1016/j.hep.2003.09.022]
8 Regev A,Berho M,Jeffers LJ,Milikowski C,Molina EG,Pyrsopoulos NT,Feng ZZ,Reddy KR,Schiff ER.Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection.Am J Gastroenterol 2002;97:2614-2618[PMID:12385448 DOI:10.1111/j.1572-0241.2002.06038.x]
9 Yin M,Talwalkar JA,Glaser KJ,Manduca A,Grimm RC,Rossman PJ,Fidler JL,Ehman RL.Assessment of hepatic fibrosis with magnetic resonance elastography.Clin Gastroenterol Hepatol2007;5:1207-1213.e2[PMID:17916548 DOI:10.1016/j.cgh.2007.06.012]
10 Batheja M,Vargas H,Silva AM,Walker F,Chang YH,De Petris G,Silva AC.Magnetic resonance elastography(MRE)in assessing hepatic fibrosis:performance in a cohort of patients with histological data.Abdom Imaging 2015;40:760-765[PMID:25542217 DOI:10.1007/s00261-014-0321-8]
11 Yoshimitsu K,Mitsufuji T,Shinagawa Y,Fujimitsu R,Morita A,Urakawa H,Hayashi H,Takano K.MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades;preliminary clinical experience.Eur Radiol 2016;26:656-663[PMID:26060066 DOI:10.1007/s00330-015-3863-4]
12 Morisaka H,Motosugi U,Ichikawa S,Sano K,Ichikawa T,Enomoto N.Association of splenic MR elastographic findings with gastroesophageal varices in patients with chronic liver disease.JMagn Reson Imaging 2015;41:117-124[PMID:24243628 DOI:10.1002/jmri.24505]
13 Talwalkar JA,Yin M,Venkatesh S,Rossman PJ,Grimm RC,Manduca A,Romano A,Kamath PS,Ehman RL.Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension.AJR Am J Roentgenol 2009;193:122-127[PMID:19542403 DOI:10.2214/AJR.07.3504]
14 Shin SU,Lee JM,Yu MH,Yoon JH,Han JK,Choi BI,Glaser KJ,Ehman RL.Prediction of esophageal varices in patients with cirrhosis:usefulness of three-dimensional MR elastography with echo-planar imaging technique.Radiology 2014;272:143-153[PMID:24620910 DOI:10.1148/radiol.14130916]
15 Nedredal GI,Yin M,McKenzie T,Lillegard J,Luebke-Wheeler J,Talwalkar J,Ehman R,Nyberg SL.Portal hypertension correlates with splenic stiffness as measured with MR elastography.JMagn Reson Imaging 2011;34:79-87[PMID:21608066 DOI:10.1002/jmri.22610]
16 Yin M,Kolipaka A,Woodrum DA,Glaser KJ,Romano AJ,Manduca A,Talwalkar JA,Araoz PA,McGee KP,Anavekar NS,Ehman RL.Hepatic and splenic stiffness augmentation assessed with MR elastography in an in vivo porcine portal hypertension model.J Magn Reson Imaging 2013;38:809-815[PMID:23418135 DOI:10.1002/jmri.24049]
17 Shin HJ,Kim HG,Kim MJ,Koh H,Kim HY,Roh YH,Lee MJ.Normal range of hepatic fat fraction on dual-and triple-echo fat quantification MR in children.PLoS One 2015;10:e0117480[PMID:25659155 DOI:10.1371/journal.pone.0117480]
18 Binkovitz LA,El-Youssef M,Glaser KJ,Yin M,Binkovitz AK,Ehman RL.Pediatric MRelastography of hepatic fibrosis:principles,technique and early clinical experience.Pediatr Radiol2012;42:402-409[PMID:22120578 DOI:10.1007/s00247-011-2298-6]
19 Xanthakos SA,Podberesky DJ,Serai SD,Miles L,King EC,Balistreri WF,Kohli R.Use of magnetic resonance elastography to assess hepatic fibrosis in children with chronic liver disease.J Pediatr 2014;164:186-188[PMID:24064151 DOI:10.1016/j.jpeds.2013.07.050]
20 Alústiza Echeverría JM,Castiella A,Emparanza JI.Quantification of iron concentration in the liver by MRI.Insights Imaging 2012;3:173-180[PMID:22696043 DOI:10.1007/s13244-011-0132-1]
21 Shneider BL,Abel B,Haber B,Karpen SJ,Magee JC,Romero R,Schwarz K,Bass LM,Kerkar N,Miethke AG,Rosenthal P,Turmelle Y,Robuck PR,Sokol RJ;Childhood Liver Disease Research and Education Network.Portal hypertension in children and young adults with biliary atresia.JPediatr Gastroenterol Nutr 2012;55:567-573[PMID:22903006 DOI:10.1097/MPG.0b013e31826eb0cf]
22 Wai CT,Greenson JK,Fontana RJ,Kalbfleisch JD,Marrero JA,Conjeevaram HS,Lok AS.Asimple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C.Hepatology 2003;38:518-526[PMID:12883497 DOI:10.1053/jhep.2003.50346]
23 North Italian Endoscopic Club for the Study and Treatment of Esophageal Varices.Prediction of the first variceal hemorrhage in patients with cirrhosis of the liver and esophageal varices.Aprospective multicenter study.N Engl J Med 1988;319:983-989[PMID:3262200 DOI:10.1056/nejm198810133191505]
24 Megremis SD,Vlachonikolis IG,Tsilimigaki AM.Spleen length in childhood with US:normal values based on age,sex,and somatometric parameters.Radiology 2004;231:129-134[PMID:14990814 DOI:10.1148/radiol.2311020963]
25 Serai SD,Towbin AJ,Podberesky DJ.Pediatric liver MR elastography.Dig Dis Sci 2012;57:2713-2719[PMID:22569825 DOI:10.1007/s10620-012-2196-2]
26 Ma X,Wang L,Wu H,Feng Y,Han X,Bu H,Zhu Q.Spleen Stiffness Is Superior to Liver Stiffness for Predicting Esophageal Varices in Chronic Liver Disease:A Meta-Analysis.PLoS One 2016;11:e0165786[PMID:27829057 DOI:10.1371/journal.pone.0165786]
27 Chongsrisawat V,Vejapipat P,Siripon N,Poovorawan Y.Transient elastography for predicting esophageal/gastric varices in children with biliary atresia.BMC Gastroenterol 2011;11:41[PMID:21501480 DOI:10.1186/1471-230X-11-41]
28 Shalaby A,Makin E,Davenport M.Portal venous pressure in biliary atresia.J Pediatr Surg 2012;47:363-366[PMID:22325391 DOI:10.1016/j.jpedsurg.2011.11.031]
29 Voutilainen S,Kivisaari R,Lohi J,Jalanko H,Pakarinen MP.A Prospective Comparison of Noninvasive Methods in the Assessment of Liver Fibrosis and Esophageal Varices in Pediatric Chronic Liver Diseases.J Clin Gastroenterol 2016;50:658-663[PMID:27105175 DOI:10.1097/MCG.0000000000000532]
30 Shin NY,Kim MJ,Lee MJ,Han SJ,Koh H,Namgung R,Park YN.Transient elastography and sonography for prediction of liver fibrosis in infants with biliary atresia.J Ultrasound Med 2014;33:853-864[PMID:24764341 DOI:10.7863/ultra.33.5.853]
31 Leschied JR,Dillman JR,Bilhartz J,Heider A,Smith EA,Lopez MJ.Shear wave elastography helps differentiate biliary atresia from other neonatal/infantile liver diseases.Pediatr Radiol 2015;45:366-375[PMID:25238807 DOI:10.1007/s00247-014-3149-z]
32 Shima H,Igarashi G,Wakisaka M,Hamano S,Nagae H,Koyama M,Kitagawa H.Noninvasive acoustic radiation force impulse(ARFI)elastography for assessing the severity of fibrosis in the post-operative patients with biliary atresia.Pediatr Surg Int 2012;28:869-872[PMID:22864589DOI:10.1007/s00383-012-3140-4]
33 Goldschmidt I,Streckenbach C,Dingemann C,Pfister ED,di Nanni A,Zapf A,Baumann U.Application and limitations of transient liver elastography in children.J Pediatr Gastroenterol Nutr2013;57:109-113[PMID:23539048 DOI:10.1097/MPG.0b013e31829206a0]
34 Yin M,Glaser KJ,Talwalkar JA,Chen J,Manduca A,Ehman RL.Hepatic MR Elastography:Clinical Performance in a Series of 1377 Consecutive Examinations.Radiology 2016;278:114-124[PMID:26162026 DOI:10.1148/radiol.2015142141]
35 Huwart L,Sempoux C,Salameh N,Jamart J,Annet L,Sinkus R,Peeters F,ter Beek LC,Horsmans Y,Van Beers BE.Liver fibrosis:noninvasive assessment with MR elastography versus aspartate aminotransferase-to-platelet ratio index.Radiology 2007;245:458-466[PMID:17940304DOI:10.1148/radiol.2452061673]
36 Trout AT,Sheridan RM,Serai SD,Xanthakos SA,Su W,Zhang B,Wallihan DB.Diagnostic Performance of MR Elastography for Liver Fibrosis in Children and Young Adults with a Spectrum of Liver Diseases.Radiology 2018;287:824-832[PMID:29470938 DOI:10.1148/radiol.2018172099]
37 Lim JK,Groszmann RJ.Transient elastography for diagnosis of portal hypertension in liver cirrhosis:is there still a role for hepatic venous pressure gradient measurement?Hepatology 2007;45:1087-1090[PMID:17464984 DOI:10.1002/hep.21731]
38 Mannelli L,Godfrey E,Joubert I,Patterson AJ,Graves MJ,Gallagher FA,Lomas DJ.MRelastography:Spleen stiffness measurements in healthy volunteers--preliminary experience.AJRAm J Roentgenol 2010;195:387-392[PMID:20651194 DOI:10.2214/AJR.09.3390]
2 Chardot C,Buet C,Serinet MO,Golmard JL,Lachaux A,Roquelaure B,Gottrand F,BrouéP,Dabadie A,Gauthier F,Jacquemin E.Improving outcomes of biliary atresia:French national series 1986-2009.J Hepatol 2013;58:1209-1217[PMID:23402746 DOI:10.1016/j.jhep.2013.01.040]
3 Hartley JL,Davenport M,Kelly DA.Biliary atresia.Lancet 2009;374:1704-1713[PMID:19914515DOI:10.1016/S0140-6736(09)60946-6]
4 Hadzi?N,Davenport M,Tizzard S,Singer J,Howard ER,Mieli-Vergani G.Long-term survival following Kasai portoenterostomy:is chronic liver disease inevitable?J Pediatr Gastroenterol Nutr2003;37:430-433[PMID:14508212]
5 Piccinino F,Sagnelli E,Pasquale G,Giusti G.Complications following percutaneous liver biopsy.A multicentre retrospective study on 68,276 biopsies.J Hepatol 1986;2:165-173[PMID:3958472]
6 Pariente D,Franchi-Abella S.Paediatric chronic liver diseases:how to investigate and follow up?Role of imaging in the diagnosis of fibrosis.Pediatr Radiol 2010;40:906-919[PMID:20432008 DOI:10.1007/s00247-010-1600-3]
7 Bedossa P,Dargère D,Paradis V.Sampling variability of liver fibrosis in chronic hepatitis C.Hepatology 2003;38:1449-1457[PMID:14647056 DOI:10.1016/j.hep.2003.09.022]
8 Regev A,Berho M,Jeffers LJ,Milikowski C,Molina EG,Pyrsopoulos NT,Feng ZZ,Reddy KR,Schiff ER.Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection.Am J Gastroenterol 2002;97:2614-2618[PMID:12385448 DOI:10.1111/j.1572-0241.2002.06038.x]
9 Yin M,Talwalkar JA,Glaser KJ,Manduca A,Grimm RC,Rossman PJ,Fidler JL,Ehman RL.Assessment of hepatic fibrosis with magnetic resonance elastography.Clin Gastroenterol Hepatol2007;5:1207-1213.e2[PMID:17916548 DOI:10.1016/j.cgh.2007.06.012]
10 Batheja M,Vargas H,Silva AM,Walker F,Chang YH,De Petris G,Silva AC.Magnetic resonance elastography(MRE)in assessing hepatic fibrosis:performance in a cohort of patients with histological data.Abdom Imaging 2015;40:760-765[PMID:25542217 DOI:10.1007/s00261-014-0321-8]
11 Yoshimitsu K,Mitsufuji T,Shinagawa Y,Fujimitsu R,Morita A,Urakawa H,Hayashi H,Takano K.MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades;preliminary clinical experience.Eur Radiol 2016;26:656-663[PMID:26060066 DOI:10.1007/s00330-015-3863-4]
12 Morisaka H,Motosugi U,Ichikawa S,Sano K,Ichikawa T,Enomoto N.Association of splenic MR elastographic findings with gastroesophageal varices in patients with chronic liver disease.JMagn Reson Imaging 2015;41:117-124[PMID:24243628 DOI:10.1002/jmri.24505]
13 Talwalkar JA,Yin M,Venkatesh S,Rossman PJ,Grimm RC,Manduca A,Romano A,Kamath PS,Ehman RL.Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension.AJR Am J Roentgenol 2009;193:122-127[PMID:19542403 DOI:10.2214/AJR.07.3504]
14 Shin SU,Lee JM,Yu MH,Yoon JH,Han JK,Choi BI,Glaser KJ,Ehman RL.Prediction of esophageal varices in patients with cirrhosis:usefulness of three-dimensional MR elastography with echo-planar imaging technique.Radiology 2014;272:143-153[PMID:24620910 DOI:10.1148/radiol.14130916]
15 Nedredal GI,Yin M,McKenzie T,Lillegard J,Luebke-Wheeler J,Talwalkar J,Ehman R,Nyberg SL.Portal hypertension correlates with splenic stiffness as measured with MR elastography.JMagn Reson Imaging 2011;34:79-87[PMID:21608066 DOI:10.1002/jmri.22610]
16 Yin M,Kolipaka A,Woodrum DA,Glaser KJ,Romano AJ,Manduca A,Talwalkar JA,Araoz PA,McGee KP,Anavekar NS,Ehman RL.Hepatic and splenic stiffness augmentation assessed with MR elastography in an in vivo porcine portal hypertension model.J Magn Reson Imaging 2013;38:809-815[PMID:23418135 DOI:10.1002/jmri.24049]
17 Shin HJ,Kim HG,Kim MJ,Koh H,Kim HY,Roh YH,Lee MJ.Normal range of hepatic fat fraction on dual-and triple-echo fat quantification MR in children.PLoS One 2015;10:e0117480[PMID:25659155 DOI:10.1371/journal.pone.0117480]
18 Binkovitz LA,El-Youssef M,Glaser KJ,Yin M,Binkovitz AK,Ehman RL.Pediatric MRelastography of hepatic fibrosis:principles,technique and early clinical experience.Pediatr Radiol2012;42:402-409[PMID:22120578 DOI:10.1007/s00247-011-2298-6]
19 Xanthakos SA,Podberesky DJ,Serai SD,Miles L,King EC,Balistreri WF,Kohli R.Use of magnetic resonance elastography to assess hepatic fibrosis in children with chronic liver disease.J Pediatr 2014;164:186-188[PMID:24064151 DOI:10.1016/j.jpeds.2013.07.050]
20 Alústiza Echeverría JM,Castiella A,Emparanza JI.Quantification of iron concentration in the liver by MRI.Insights Imaging 2012;3:173-180[PMID:22696043 DOI:10.1007/s13244-011-0132-1]
21 Shneider BL,Abel B,Haber B,Karpen SJ,Magee JC,Romero R,Schwarz K,Bass LM,Kerkar N,Miethke AG,Rosenthal P,Turmelle Y,Robuck PR,Sokol RJ;Childhood Liver Disease Research and Education Network.Portal hypertension in children and young adults with biliary atresia.JPediatr Gastroenterol Nutr 2012;55:567-573[PMID:22903006 DOI:10.1097/MPG.0b013e31826eb0cf]
22 Wai CT,Greenson JK,Fontana RJ,Kalbfleisch JD,Marrero JA,Conjeevaram HS,Lok AS.Asimple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C.Hepatology 2003;38:518-526[PMID:12883497 DOI:10.1053/jhep.2003.50346]
23 North Italian Endoscopic Club for the Study and Treatment of Esophageal Varices.Prediction of the first variceal hemorrhage in patients with cirrhosis of the liver and esophageal varices.Aprospective multicenter study.N Engl J Med 1988;319:983-989[PMID:3262200 DOI:10.1056/nejm198810133191505]
24 Megremis SD,Vlachonikolis IG,Tsilimigaki AM.Spleen length in childhood with US:normal values based on age,sex,and somatometric parameters.Radiology 2004;231:129-134[PMID:14990814 DOI:10.1148/radiol.2311020963]
25 Serai SD,Towbin AJ,Podberesky DJ.Pediatric liver MR elastography.Dig Dis Sci 2012;57:2713-2719[PMID:22569825 DOI:10.1007/s10620-012-2196-2]
26 Ma X,Wang L,Wu H,Feng Y,Han X,Bu H,Zhu Q.Spleen Stiffness Is Superior to Liver Stiffness for Predicting Esophageal Varices in Chronic Liver Disease:A Meta-Analysis.PLoS One 2016;11:e0165786[PMID:27829057 DOI:10.1371/journal.pone.0165786]
27 Chongsrisawat V,Vejapipat P,Siripon N,Poovorawan Y.Transient elastography for predicting esophageal/gastric varices in children with biliary atresia.BMC Gastroenterol 2011;11:41[PMID:21501480 DOI:10.1186/1471-230X-11-41]
28 Shalaby A,Makin E,Davenport M.Portal venous pressure in biliary atresia.J Pediatr Surg 2012;47:363-366[PMID:22325391 DOI:10.1016/j.jpedsurg.2011.11.031]
29 Voutilainen S,Kivisaari R,Lohi J,Jalanko H,Pakarinen MP.A Prospective Comparison of Noninvasive Methods in the Assessment of Liver Fibrosis and Esophageal Varices in Pediatric Chronic Liver Diseases.J Clin Gastroenterol 2016;50:658-663[PMID:27105175 DOI:10.1097/MCG.0000000000000532]
30 Shin NY,Kim MJ,Lee MJ,Han SJ,Koh H,Namgung R,Park YN.Transient elastography and sonography for prediction of liver fibrosis in infants with biliary atresia.J Ultrasound Med 2014;33:853-864[PMID:24764341 DOI:10.7863/ultra.33.5.853]
31 Leschied JR,Dillman JR,Bilhartz J,Heider A,Smith EA,Lopez MJ.Shear wave elastography helps differentiate biliary atresia from other neonatal/infantile liver diseases.Pediatr Radiol 2015;45:366-375[PMID:25238807 DOI:10.1007/s00247-014-3149-z]
32 Shima H,Igarashi G,Wakisaka M,Hamano S,Nagae H,Koyama M,Kitagawa H.Noninvasive acoustic radiation force impulse(ARFI)elastography for assessing the severity of fibrosis in the post-operative patients with biliary atresia.Pediatr Surg Int 2012;28:869-872[PMID:22864589DOI:10.1007/s00383-012-3140-4]
33 Goldschmidt I,Streckenbach C,Dingemann C,Pfister ED,di Nanni A,Zapf A,Baumann U.Application and limitations of transient liver elastography in children.J Pediatr Gastroenterol Nutr2013;57:109-113[PMID:23539048 DOI:10.1097/MPG.0b013e31829206a0]
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